Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Molecular Medicine Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1791-2997 Online ISSN: 1791-3004
Journal Cover
February-2018 Volume 17 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
February-2018 Volume 17 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article Open Access

Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation

  • Authors:
    • Kai Le Pang
    • Kavitha Vijayaraghavan
    • Badr Al Sayed
    • Mohamed Ali Seyed
  • View Affiliations / Copyright

    Affiliations: Faculty of Pharmacy, Universiti, Kebangsaan Malaysia (UKM), The National University of Malaysia, Kuala Lumpur 50300, Malaysia, Agni College of Technology, Thalambur, Chennai 600 130, India, Faculty of Medicine, University of Tabuk, Tabuk 71491, Saudi Arabia
    Copyright: © Pang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 3035-3041
    |
    Published online on: December 12, 2017
       https://doi.org/10.3892/mmr.2017.8262
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

The aim of the present study was to investigate the effects of betulinic acid (BetA) on the expression and distribution pattern of nicotinamide adenine dinucleotide phosphate diaphorase (NADPH‑d), an indirect indicator of nitric oxide (NO) synthase in the thymus and spleen of mice. Mice were randomly assigned to four main groups (n=48 per group): Experimental group (BetA), positive control group (goniothalamin), vehicle control group (dimethyl sulfoxide) and control group (without vehicle). Each group was further divided into three equal subgroups according to the treatment length (4, 8 and 12 days). BetA treatment induced the expression of NADPH‑d activity in the thymus and spleen without any significant changes in the morphology of the organs. Furthermore, the expression pattern of NADPH‑d in BetA‑treated animals was significantly increased compared with that in the control animals. NADPH‑d expression in the thymus and spleen suggests that NO signaling may be a potential mechanism underlying the BetA‑induced immunomodulation in these organs. These findings are of direct clinical relevance and may contribute to the further development of BetA as a therapeutic drug.
View Figures

Figure 1

Figure 2

Figure 3

View References

1 

Geetha S, Singh V, Ram MS, Ilavazhagan G, Banerjee PK and Sawhney RC: Immunomodulatory effects of seabuckthorn (Hippophae rhamnoides L.) against chromium (VI) induced immunosuppression. Mol Cell Biochem. 278:101–109. 2005. View Article : Google Scholar : PubMed/NCBI

2 

Aravindaram K and Yang NS: Anti-inflammatory plant natural products for cancer therapy. Planta Med. 76:1103–1117. 2010. View Article : Google Scholar : PubMed/NCBI

3 

Winkler C, Wirleitner B, Schroecksnadel K, Schennach H, Mur E and Fuchs D: In vitro effects of two extracts and two pure alkaloid preparations of Uncaria tomentosa on peripheral blood mononuclear cells. Planta Med. 70:205–210. 2004. View Article : Google Scholar : PubMed/NCBI

4 

Patwardhan B and Gautam M: Botanical immunodrugs: Scope and opportunities. Drug Discov Today. 10:495–502. 2005. View Article : Google Scholar : PubMed/NCBI

5 

Sreesha T: In-vitro study of cytotoxicity activity of flavonoid fraction from the petals of Cassia senna. Int J Ethnomed Pharmacol Res. 1:52–55. 2013.

6 

Nagarathna PKM, Reena K, Sriram Reddy and Johnson W: Review on immunomodulation and immunomodulatory activity of some herbal plants. Int J Pharm Sci Rev Res. 22:223–230. 2013.

7 

Ibrahim J, Waqas A and Syed Nasir AB: Plant-derived immunomodulators: An insight on their preclinical evaluation and clinical trials. Front Plant Sci. 6:6552015.PubMed/NCBI

8 

Schepetkin IA and Quinn MT: Botanical polysaccharides: Macrophage immunomodulation and therapeutic potential. Int Immunopharmacol. 6:317–333. 2006. View Article : Google Scholar : PubMed/NCBI

9 

Eiznhamer DA and Xu ZQ: Betulinic acid: A promising anticancer candidate. IDrugs. 7:359–373. 2004.PubMed/NCBI

10 

Higa M, Noha N, Yokaryo H, Ogihara K and Yogi S: Three new naphthoquinone derivatives from Diospyros maritima Blume. Chem Pharm Bull (Tokyo). 50:590–593. 2002. View Article : Google Scholar : PubMed/NCBI

11 

Hanson JR: Pentacyclic triterpenes as promising agents in cancer. Salvador JAR: Nova Science Publishers, Inc; New York, NY: pp. 1912010

12 

Santos RC, Salvador JA, Marín S, Cascante M, Moreira JN and Dinis TC: Synthesis and structure-activity relationship study of novel cytotoxic carbamate and N-acylheterocyclic bearing derivatives of betulin and betulinic acid. Bioorg Med Chem. 18:4385–4396. 2010. View Article : Google Scholar : PubMed/NCBI

13 

Zhang DM, Xu HG, Wang L, Li YJ, Sun PH, Wu XM, Wang GJ, Chen WM and Ye WC: Betulinic acid and its derivatives as potential antitumor agents. Med Res Rev. 35:1127–1155. 2015. View Article : Google Scholar : PubMed/NCBI

14 

Ali-Seyed M, Jantan I, Vijayaraghavan K and Bukhari SN: Betulinic acid: Recent advances in chemical modifications, effective delivery, and molecular mechanisms of a promising anticancer therapy. Chem Biol Drug Des. 87:517–536. 2016. View Article : Google Scholar : PubMed/NCBI

15 

Alakurtti S, Mäkelä T, Koskimies S and Yli-Kauhaluoma J: Pharmacological properties of the ubiquitous natural product betulin. Eur J Pharm Sci. 29:1–13. 2006. View Article : Google Scholar : PubMed/NCBI

16 

Csuk R: Betulinic acid and its derivatives: A patent review (2008–2013). Expert Opin Ther Pat. 24:913–923. 2014. View Article : Google Scholar : PubMed/NCBI

17 

Zuco V, Supino R, Righetti SC, Cleris L, Marchesi E, Gambacorti-Passerini C and Formelli F: Selective cytotoxicity of betulinic acid on tumor cell lines, but not on normal cells. Cancer Lett. 175:17–25. 2002. View Article : Google Scholar : PubMed/NCBI

18 

Thurnher D, Turhani D, Pelzmann M, Wannemacher B, Knerer B, Formanek M, Wacheck V and Selzer E: Betulinic acid: A new cytotoxic compound against malignant head and neck cancer cells. Head Neck. 25:732–740. 2003. View Article : Google Scholar : PubMed/NCBI

19 

Mukherjee R, Kumar V, Srivastava SK, Agarwal SK and Burman AC: Betulinic acid derivatives as anticancer agents: Structure activity relationship. Anticancer Agents Med Chem. 6:271–279. 2006. View Article : Google Scholar : PubMed/NCBI

20 

Galgon T, Wohlrab W and Dräger B: Betulinic acid induces apoptosis in skin cancer cells and differentiation in normal human keratinocytes. Exp Dermatol. 14:736–743. 2005. View Article : Google Scholar : PubMed/NCBI

21 

Selzer E, Pimentel E, Wacheck V, Schlegel W, Pehamberger H, Jansen B and Kodym R: Effects of betulinic acid alone and in combination with irradiation in human melanoma cells. J Invest Dermatol. 114:935–940. 2000. View Article : Google Scholar : PubMed/NCBI

22 

Periasamy G, Teketelew G, Gebrelibanos M, Sintayehu B, Gebrehiwot M, Karim A and Geremedhin G: Betulinic acid and its derivatives as anti-cancer agent: A review. Arch Appl Sci Res. 6:47–58. 2014.

23 

Mullauer FB, Kessler JH and Medema JP: Betulinic acid, a natural compound with potent anticancer effects. Anticancer Drugs. 21:215–227. 2010. View Article : Google Scholar : PubMed/NCBI

24 

Heiss EH, Kramer MP, Atanasov AG, Beres H, Schachner D and Dirsch VM: Glycolytic switch in response to betulinic acid in non-cancer cells. PLoS One. 9:e1156832014. View Article : Google Scholar : PubMed/NCBI

25 

Moncada S, Palmer RM and Higgs A: Nitric oxide: Physiology, pathophysiology and pharmacology. Pharmacol Rev. 43:109–142. 1991.PubMed/NCBI

26 

Knowles RG and Moncada S: Nitric oxide synthase in mammals. Biochemical J. 298:249–258. 1994. View Article : Google Scholar

27 

Syed MA, Leong SK and Chan AS: Localization of NADPH-diaphorase reactivity in the chick and mouse thyroid gland. Thyroid. 4:475–478. 1994. View Article : Google Scholar : PubMed/NCBI

28 

Gulati P, Leong SK and Chan AS: Ontogeny of NADPH-d expression in the thymic microenvironment of the chick embryo. Cell Tissue Res. 294:335–343. 1998. View Article : Google Scholar : PubMed/NCBI

29 

Akbari Z, Rohani MH and Behzadi G: NADPH-d/NOS reactivity in the lumbar dorsal horn of congenitally hypothyroid pups before and after formalin pain induction. Int J Dev Neurosci. 27:779–787. 2009. View Article : Google Scholar : PubMed/NCBI

30 

Förstermann U and Sessa WC: Nitric oxide synthases: Regulation and function. Eur Heart J. 33:829–837, 837a-837d. 2012. View Article : Google Scholar : PubMed/NCBI

31 

Andronowska A and Chruściel M: Expression and cellular distribution of NADPH-diaphorase and nitric oxide synthases in the porcine uterus during early pregnancy. Folia Histochem Cytobiol. 45:375–380. 2007.PubMed/NCBI

32 

Ali SM, Chan AS and Leong SK: Localization of nitrergic neuronal and non-neuronal cells in the ultimobranchial glands of the chicken. Anat Embryol (Berl). 193:161–168. 1996. View Article : Google Scholar : PubMed/NCBI

33 

Dorko F, Špakovská T, Lovasová K, Patlevič P and Kluchová D: NADPH-d activity in rat thymus after the application of retinoid acid. Eur J Histochem. 56:e72012. View Article : Google Scholar : PubMed/NCBI

34 

Hope BT, Michael GJ, Knigge KM and Vincent SR: Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA. 88:pp. 2811–2814. 1991; View Article : Google Scholar : PubMed/NCBI

35 

Steiniger BS: Human spleen microanatomy: Why mice do not suffice. Immunology. 145:334–346. 2015. View Article : Google Scholar : PubMed/NCBI

36 

Danko J, Ondrasovic M, Svický E, Jenca A, Pospieszny N and Ondrasovicová O: Histochemical study of innervation and NADPH-D activity of the thymus. Anat Histol Embryol. 32:233–235. 2003. View Article : Google Scholar : PubMed/NCBI

37 

Svický E, Ondraovic M, Danko J, Ondrasovicová O, Jenca A, Pospieszny N and Toropila M: Localisation of NADPH-diaphorase-positive structures in the thymus of the rat, mouse and rabbit. Folia Morphol (Warsz). 62:167–170. 2003.PubMed/NCBI

38 

Jacobs AT and Ignarro LJ: Lipopolysaccharide-induced expression of interferon-beta mediates the timing of inducible nitric-oxide synthase induction in RAW 264.7 macrophages. J Biol Chem. 276:47950–47957. 2001. View Article : Google Scholar : PubMed/NCBI

39 

Yi JE, Obminska-Mrukowicz B, Yuan LY and Yuan H: Immunomodulatory effects of betulinic acid from the bark of white birch on mice. J Vet Sci. 11:305–313. 2010. View Article : Google Scholar : PubMed/NCBI

40 

Jine Y, Lis M, Szczypka M and Obmińska-Mrukowicz B: Influence of betulinic acid on lymphocyte subsets and humoral immune response in mice. Pol J Vet Sci. 15:305–313. 2012.PubMed/NCBI

41 

Hibbs JB Jr: Infection and nitric oxide. J Infect Dis. 185 Suppl 1:S9–S17. 2002. View Article : Google Scholar : PubMed/NCBI

42 

Ibiza S and Serrador JM: The role of nitric oxide in the regulation of adaptive immune responses. Immunología. 27:103–117. 2008.

43 

Filep JG, Földes-Filep E, Rousseau A, Sirois P and Fournier A: Vascular responses to endothelin-1 following inhibition of nitric oxide synthesis in the conscious rat. Br J Pharmacol. 110:1213–1221. 1993. View Article : Google Scholar : PubMed/NCBI

44 

Umeshappa CS, Singh KP, Nanjundappa RH, Channappanavar R, Maan S and Maan NS: Bluetongue virus-23 stimulates inducible nitric oxide synthase expression and nitric oxide production in mononuclear cells of blood and/or regional lymphoid organs. Vet Res Commun. 36:245–250. 2012. View Article : Google Scholar : PubMed/NCBI

45 

Darwiche SS, Pfeifer R, Menzel C, Ruan X, Hoffman M, Cai C, Chanthaphavong RS, Loughran P, Pitt BR, Hoffman R, et al: Inducible nitric oxide synthase contributes to immune dysfunction following trauma. Shock. 38:499–507. 2012. View Article : Google Scholar : PubMed/NCBI

46 

Zdzisińska B, Rzeski W, Paduch R, Szuster-Ciesielska A, Kaczor J, Wejksza K and Kandefer-Szerszeń M: Differential effect of betulin and betulinic acid on cytokine production in human whole blood cell cultures. Pol J Pharmacol. 55:235–238. 2003.PubMed/NCBI

47 

Chen S, Bai Y, Li Z, Jia K, Jin Y, He B, Qiu WW, Du C, Siwko S, Chen H, et al: A betulinic acid derivative SH479 inhibits collagen-induced arthritis by modulating T cell differentiation and cytokine balance. Biochem Pharmacol. 126:69–78. 2017. View Article : Google Scholar : PubMed/NCBI

48 

Sultana N and Saify ZS: Naturally occurring and synthetic agents as potential anti-inflammatory and immunomodulants. Antiinflamm Antiallergy Agents Med Chem. 11:3–19. 2012. View Article : Google Scholar : PubMed/NCBI

49 

Wang P, Li Q, Li K, Zhang X, Han Z, Wang J, Gao D and Li J: Betulinic acid exerts immunoregulation and anti-tumor effect on cervical carcinoma (U14) tumor-bearing mice. Pharmazie. 67:733–739. 2012.PubMed/NCBI

50 

Dash SK, Chattopadhyay S, Tripathy S, Dash SS, Das B, Mandal D, Mahapatra SK, Bag BG and Roy S: Self-assembled betulinic acid augments immunomodulatory activity associates with IgG response. Biomed Pharmacother. 75:205–217. 2015. View Article : Google Scholar : PubMed/NCBI

51 

Yi J, Zhu R, Wu J, Wu J, Xia W, Zhu L, Jiang W, Xiang S and Tan Z: In vivo protective effect of betulinic acid on dexamethasone induced thymocyte apoptosis by reducing oxidative stress. Pharmacol Rep. 68:95–100. 2016. View Article : Google Scholar : PubMed/NCBI

52 

Kovalenko LP, Balakshin VV, Presnova GA, Chistyakov AN, Shipaeva EV, Alekseeva SV and Durnev AD: Immunotoxicity and allergenic properties of betulin-containing birch bark dry extract. Pharm Chem J. 41:17–19. 2007. View Article : Google Scholar

53 

Naithani R, Huma LC, Moriarty RM, McCormick DL and Mehta RG: Comprehensive review of cancer chemopreventive agents evaluated in experimental carcinogenesis models and clinical trials. Curr Med Chem. 15:1044–1071. 2008. View Article : Google Scholar : PubMed/NCBI

54 

Paszkiewicz M, Budzyńska A, Różalska B and Sadowska B: The immunomodulatory role of plant polyphenols. Postepy Hig Med Dosw (Online). 66:637–636. 2012.(In Polish). View Article : Google Scholar : PubMed/NCBI

55 

Mathew NS and Negi PS: Traditional uses, phytochemistry and pharmacology of wild Banana (Musa acuminata Colla): A review. J Ethnopharmacol. 196:124–140. 2017. View Article : Google Scholar : PubMed/NCBI

56 

Schmidt A, Bilgasem S, Lorkowski S, Vischer P, Völker W, Breithardt G, Siegel G and Buddecke E: Exogenous nitric oxide regulates activity and synthesis of vascular endothelial nitric oxide synthase. Eur J Clin Invest. 38:476–485. 2008. View Article : Google Scholar : PubMed/NCBI

57 

Son Y, Lee JH, Cheong YK, Jung HC, Jeong SO, Park SH and Pae HO: Piceatannol, a natural hydroxylated analog of resveratrol, promotes nitric oxide release through phosphorylation of endothelial nitric oxide synthase in human endothelial cells. Eur Rev Med Pharmacol Sci. 19:3125–3132. 2015.PubMed/NCBI

58 

Tillery LC, Epperson TA, Eguchi S and Motley ED: Differential regulation of endothelial nitric oxide synthase phosphorylation by protease-activated receptors in adult human endothelial cells. Exp Biol Med (Maywood). 241:569–580. 2016. View Article : Google Scholar : PubMed/NCBI

59 

Steinkamp-Fenske K, Bollinger L, Xu H, Yao Y, Horke S, Förstermann U and Li H: Reciprocal regulation of endothelial nitric-oxide synthase and NADPH oxidase by betulinic acid in human endothelial cells. J Pharmacol Exp Ther. 322:836–842. 2007. View Article : Google Scholar : PubMed/NCBI

60 

Qian LB, Fu JY, Cai X and Xia ML: Betulinic acid inhibits superoxide anion-mediated impairment of endothelium-dependent relaxation in rat aortas. Ind J Pharmacol. 44:588–592. 2012. View Article : Google Scholar

61 

Hohmann N, Xia N, Steinkamp-Fenske K, Förstermann U and Li H: Estrogen receptor signaling and the PI3K/Akt pathway are involved in betulinic acid-induced eNOS activation. Molecules. 21:E9732016. View Article : Google Scholar : PubMed/NCBI

62 

Jin SW, Choi CY, Hwang YP, Kim HG, Kim SJ, Chung YC, Lee KJ, Jeong TC and Jeong HG: Betulinic acid increases eNOS phosphorylation and no synthesis via the calcium-signaling pathway. J Agric Food Chem. 64:785–791. 2016. View Article : Google Scholar : PubMed/NCBI

63 

Chen MF, Huang YC, Long C, Yang HI, Lee HC, Chen PY, Hoffer BJ and Lee TJ: Bimodal effects of fluoxetine on cerebral nitrergic neurogenic vasodilation in porcine large cerebral arteries. Neuropharmacology. 62:1651–1658. 2012. View Article : Google Scholar : PubMed/NCBI

64 

Lies B, Beck K, Keppler J, Saur D, Groneberg D and Friebe A: Nitrergic signalling via interstitial cells of Cajal regulates motor activity in murine colon. J Physiol. 593:4589–4601. 2015. View Article : Google Scholar : PubMed/NCBI

65 

Wenisch S and Arnhold S: NADPH-diaphorase activity and NO synthase expression in the olfactory epithelium of the bovine. Anat Histol Embryol. 39:201–206. 2010. View Article : Google Scholar : PubMed/NCBI

66 

Şelaru M, Rusu MC and Jianu AM: Expression of nNOS in the human larynx. Anat Sci Int. 90:327–330. 2015. View Article : Google Scholar : PubMed/NCBI

67 

Knipping S, Holzhausen HJ, Berghaus A, Bloching M and Riederer A: Ultrastructural detection of nitric oxide in human nasal mucosa. Otolaryngol Head Neck Surg. 132:620–625. 2005. View Article : Google Scholar : PubMed/NCBI

68 

Koyama T, Hatanaka Y, Jin X, Yokomizo A, Fujiwara H, Goda M, Hobara N, Zamami Y, Kitamura Y and Kawasaki H: Altered function of nitrergic nerves inhibiting sympathetic neurotransmission in mesenteric vascular beds of renovascular hypertensive rats. Hypertens Res. 33:485–491. 2010. View Article : Google Scholar : PubMed/NCBI

69 

Shimada S, Todoki K, Omori Y, Toyama T, Matsuo M, Wada-Takahashi S, Takahashi SS and Lee MC: Contribution of nitrergic nerve in canine gingival reactive hyperemia. J Clin Biochem Nutr. 56:98–104. 2015. View Article : Google Scholar : PubMed/NCBI

70 

Mignini F, Sabbatini M, D'Andrea V and Cavallotti C: Intrinsic innervation and dopaminergic markers after experimental denervation in rat thymus. Eur J Histochem. 54:e172010. View Article : Google Scholar : PubMed/NCBI

71 

Dorko F, Danko J, Flešárová S, Boroš E and Sobeková A: Effect of pesticide bendiocar-bamate on distribution of acetylcholine- and butyrylcholine-positive nerves in rabbit's thymus. Eur J Histochem. 55:e372011. View Article : Google Scholar : PubMed/NCBI

72 

Liu C, Yang Y, Hu X, Li JM, Zhang XM, Cai Y, Li Z and Yan XX: Ontogenesis of NADPH-diaphorase positive neurons in guinea pig neocortex. Front Neuroanat. 9:112015. View Article : Google Scholar : PubMed/NCBI

73 

Jung J, Na C and Huh Y: Alterations in nitric oxide synthase in the aged CNS. Oxid Med Cell Longev. 2012:7189762012. View Article : Google Scholar : PubMed/NCBI

74 

Cossenza M, Socodato R, Portugal CC, Domith IC, Gladulich LF, Encarnação TG, Calaza KC, Mendonça HR, Campello-Costa P and Paes-de-Carvalho R: Nitric oxide in the nervous system: Biochemical, developmental, and neurobiological aspects. Vitam Horm. 96:79–125. 2014. View Article : Google Scholar : PubMed/NCBI

75 

Downing JE: Multiple nitric oxide synthase systems in adult rat thymus revealed using NADPH diaphorase histochemistry. Immunology. 82:659–664. 1994.PubMed/NCBI

76 

Villanueva C and Giulivi C: Subcellular and cellular locations of nitric-oxide synthase isoforms as determinants of health and disease. Free Radic Biol Med. 49:307–316. 2010. View Article : Google Scholar : PubMed/NCBI

77 

Bogdan C: Nitric oxide synthase in innate and adaptive immunity: An update. Trends Immunol. 36:161–178. 2015. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Pang K, Vijayaraghavan K, Al Sayed B and Seyed M: Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation. Mol Med Rep 17: 3035-3041, 2018.
APA
Pang, K., Vijayaraghavan, K., Al Sayed, B., & Seyed, M. (2018). Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation. Molecular Medicine Reports, 17, 3035-3041. https://doi.org/10.3892/mmr.2017.8262
MLA
Pang, K., Vijayaraghavan, K., Al Sayed, B., Seyed, M."Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation". Molecular Medicine Reports 17.2 (2018): 3035-3041.
Chicago
Pang, K., Vijayaraghavan, K., Al Sayed, B., Seyed, M."Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation". Molecular Medicine Reports 17, no. 2 (2018): 3035-3041. https://doi.org/10.3892/mmr.2017.8262
Copy and paste a formatted citation
x
Spandidos Publications style
Pang K, Vijayaraghavan K, Al Sayed B and Seyed M: Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation. Mol Med Rep 17: 3035-3041, 2018.
APA
Pang, K., Vijayaraghavan, K., Al Sayed, B., & Seyed, M. (2018). Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation. Molecular Medicine Reports, 17, 3035-3041. https://doi.org/10.3892/mmr.2017.8262
MLA
Pang, K., Vijayaraghavan, K., Al Sayed, B., Seyed, M."Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation". Molecular Medicine Reports 17.2 (2018): 3035-3041.
Chicago
Pang, K., Vijayaraghavan, K., Al Sayed, B., Seyed, M."Betulinic acid‑induced expression of nicotinamide adenine dinucleotide phosphate‑diaphorase in the immune organs of mice: A possible role of nitric oxide in immunomodulation". Molecular Medicine Reports 17, no. 2 (2018): 3035-3041. https://doi.org/10.3892/mmr.2017.8262
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team