Concentration of tissue angiotensin II increases with severity of experimental pancreatitis

Furukawa,Hiroyuki; Shinmura,Atsushi; Tajima,Hidehiro; Tsukada,Tomoya; Nakanuma,Shin‑Ichi; Okamoto,Koichi; Sakai,Seisho; Makino,Isamu; Nakamura,Keishi; Hayashi,Hironori; Oyama,Katsunobu; Inokuchi,Masafumi; Nakagawara,Hisatoshi; Miyashita,Tomoharu; Fujita,Hideto; Takamura,Hiroyuki; Ninomiya, Itasu; Kitagawa,Hirohisa; Fushida,Sachio; Fujimura,Takashi; Ohta,Tetsuo; Wakayama,Tomohiko; Iseki,Shoichi

doi:10.3892/mmr.2013.1509

August 2013 Volume 8 Issue 2

Full Size Image

Journals

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 is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

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

Oncology Reports

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

Experimental and Therapeutic Medicine

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

Oncology Letters

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

Biomedical Reports

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

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

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

International Journal of Functional Nutrition

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

International Journal of Epigenetics

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

Medicine International

An International Open Access Journal Devoted to General Medicine.

August 2013 Volume 8 Issue 2

Full Size Image

Article

Concentration of tissue angiotensin II increases with severity of experimental pancreatitis

Authors:
- Hiroyuki Furukawa
- Atsushi Shinmura
- Hidehiro Tajima
- Tomoya Tsukada
- Shin‑Ichi Nakanuma
- Koichi Okamoto
- Seisho Sakai
- Isamu Makino
- Keishi Nakamura
- Hironori Hayashi
- Katsunobu Oyama
- Masafumi Inokuchi
- Hisatoshi Nakagawara
- Tomoharu Miyashita
- Hideto Fujita
- Hiroyuki Takamura
- Itasu Ninomiya
- Hirohisa Kitagawa
- Sachio Fushida
- Takashi Fujimura
- Tetsuo Ohta
- Tomohiko Wakayama
- Shoichi Iseki
View Affiliations / Copyright

Affiliations: Department of Gastroenterological Surgery, Division of Cancer Medicine, Graduate School of Medical Science, Kanazawa University, Kanazawa, Ishikawa 920‑8641, Japan, Department of Histology and Embryology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Ishikawa 920‑8641, Japan
Pages: 335-338
|
Published online on: June 6, 2013

https://doi.org/10.3892/mmr.2013.1509
Expand metrics +

Abstract

Necrotizing pancreatitis is a serious condition that is associated with high morbidity and mortality. Although vasospasm is reportedly involved in necrotizing pancreatitis, the underlying mechanism is not completely clear. In addition, the local renin‑angiotensin system has been hypothesized to be involved in the progression of pancreatitis and trypsin has been shown to generate angiotensin II under weakly acidic conditions. However, to the best of our knowledge, no studies have reported elevated angiotensin II levels in tissue with pancreatitis. In the present study, the concentration of pancreatic angiotensin II in rats with experimentally induced acute pancreatitis was measured. Acute pancreatitis was induced by retrograde injection of 6% sodium taurocholate into the biliopancreatic duct. Control rats were sacrificed without injection into the biliopancreatic duct. The concentration of tissue angiotensin II was measured using the florisil method. Angiotensin II concentration in tissues with acute pancreatitis measured at 3, 6, 12 and 24 h following taurocholate injection were significantly higher than that of normal pancreatic tissue. In addition, the concentration of angiotensin II increased in a time‑dependent manner. The results demonstrated that the angiotensin II generating system is involved in the transition from edematous to necrotizing pancreatitis in experimental animals. We hypothesize that locally formed angiotensin II affects the microenvironment in pancreatitis.

View Figures

View References

1	Bollen TL, van Santvoort HC, Besselink MG, et al: The Atlanta Classification of acute pancreatitis revisited. Br J Surg. 95:6–21. 2008. View Article : Google Scholar : PubMed/NCBI
2	Traverso LW and Kozarek RA: Pancreatic necrosectomy: definitions and technique. J Gastrointest Surg. 9:436–439. 2005. View Article : Google Scholar : PubMed/NCBI
3	Takeda K, Mikami Y, Fukuyama S, et al: Pancreatic ischemia associated with vasospasm in the early phase of human acute necrotizing pancreatitis. Pancreas. 30:40–49. 2005.PubMed/NCBI
4	Paul M, Poyan Mehr A and Kreutz R: Physiology of local renin-angiotensin systems. Physiol Rev. 86:747–803. 2006. View Article : Google Scholar : PubMed/NCBI
5	Chappell MC, Millsted A, Diz DI, et al: Evidence for an intrinsic angiotensin system in the carine pancreas. J Hypertens. 9:751–759. 1991. View Article : Google Scholar : PubMed/NCBI
6	Chappell MC, Jacobsen DW and Tallant EA: Characterization of angiotensin II receptor subtypes in pancreatic acinar AR42J cells. Peptides. 16:741–747. 1995. View Article : Google Scholar
7	Ghiani BU and Masini MA: Angiotensin II binding sites in the rat pancreas and their modulation after sodium. Comp Biochem Physiol A Physiol. 111:439–444. 1995. View Article : Google Scholar : PubMed/NCBI
8	Leung PS, Chan WP, Wong TP, et al: Expression and localization of the renin-angiotensin system in the rat pancreas. J Endocrinol. 160:13–19. 1999. View Article : Google Scholar : PubMed/NCBI
9	Tahmasebi M, Puddefoot JR, Inwang ER, et al: The tissue renin-angiotensin system in human pancreas. J Endocrinol. 161:317–322. 1999. View Article : Google Scholar : PubMed/NCBI
10	Leung PS, Chan WP and Nobiling R: Regulated expression of pancreatic renin-angiotensin system in experimental pancreatitis. Mol Cell Endocrinol. 166:121–128. 2000. View Article : Google Scholar : PubMed/NCBI
11	Ip SP, Kwan PC, Williams CH, et al: Changes of angiotensin-converting enzyme activity in the pancreas of chronic hypoxia and acute pancreatitis. Int J Biochem Cell Biol. 35:944–954. 2003. View Article : Google Scholar : PubMed/NCBI
12	Arakawa K, Ikeda M, Fukuyama J, et al: A pressor formation by trypsin from renin-denatured human plasma protein. J Clin Endocrinol Metab. 42:599–602. 1976. View Article : Google Scholar : PubMed/NCBI
13	Arakawa K and Maruta H: Ability of kallikrein to generate angiotensin II-like pressor substance and a proposed ‘kinin-tensin enzyme system’. Nature. 288:705–706. 1980.PubMed/NCBI
14	Morimoto T, Aoyama M, Gotoh E, et al: A method of radioimmunoassay of plasma angiotensin II using florisil. Nihon Naibunpi Gakkai Zasshi. 59:15–29. 1983.(In Japanese).
15	Spormann H, Sokolowski A and Letko G: Effect of temporary ischemia upon development and histological patterns of acute pancreatitis in the rat. Pathol Res Pract. 184:507–513. 1989. View Article : Google Scholar : PubMed/NCBI
16	Klar E, Rattner DW, Compton C, et al: Adverse effect of theraeuic vasoconstrictors in experimental acute pancreatitis. Ann Surg. 214:168–174. 1991. View Article : Google Scholar : PubMed/NCBI
17	Menger MD, Plusczyk T and Vollmar B: Microcirculatory derangements in acute pancreatitis. J Hepatobiliary Pancreat Surg. 8:187–194. 2001. View Article : Google Scholar : PubMed/NCBI
18	Liu XH, Kimura T, Ishikawa H, et al: Effect of endothelin-1 on the decelopment of hemorrhagic pancreatitis in rats. Scand J Gastroenterol. 30:276–282. 1995. View Article : Google Scholar : PubMed/NCBI
19	Foitzik T, Faulhaber J, Hotz HG, et al: Endothelin mediates local and systemic disease sequelae in severe experimental pancreatitis. Pancreas. 22:248–254. 2001. View Article : Google Scholar : PubMed/NCBI
20	Chan WP, Fung ML, Nobiling R, et al: Activation of local renin-angiotensin system by chronic hypoxia in rat pancreas. Mol Cell Endocrinol. 160:107–114. 2000. View Article : Google Scholar : PubMed/NCBI
21	Tsang SW, Cheng CH and Leung PS: The role of the pancreatic rennin-angiotensin system in acinar digestive enzyme secretion and in acute pancreatitis. Regul Pept. 119:213–219. 2004. View Article : Google Scholar : PubMed/NCBI
22	Chan YC and Leung PS: Angiotensin II type 1 receptor-dependent nuclear factor-kB activation-mediated proinflammatory actions in a rat model of obstructive acute pancreatitis. J Pharmacol Exp Ther. 323:10–18. 2007. View Article : Google Scholar : PubMed/NCBI
23	Oruc N, Ozutemiz O, Nart D, et al: Inhibition of renin-angiotensin systems in experimental acute pancreatitis in rats: A new therapeutic target? Exp Toxicol Pathol. 62:353–360. 2010. View Article : Google Scholar : PubMed/NCBI
24	Figarella C, Miszczuk-Jamska B and Barrett AJ: Possible lysosomal activation of pancreatic zymogens. Activation of both human trypsinogens by cathepsin B and spontaneous acid Activation of human trypsinogen 1. Biol Chem Hoppe Seyler. 369:293–298. 1988.PubMed/NCBI
25	Tajima H, Ohta T, Elnemr A, et al: Enhanced incasiveness of pancreatic adenocarcinoma cells stably transfected with cationic trypsinogen cDNA. Int J Cancer. 94:699–704. 2001. View Article : Google Scholar : PubMed/NCBI
26	Ohta T, Amaya K, Yi S, et al: Angiotensin converting enzyme-independent, local angiotensin II-generation in human pancreatic ductal cancer tissue. Int J Oncol. 23:593–598. 2003.PubMed/NCBI
27	Montcourrier P, Silver I, Farnoud R, et al: Breast cancer cells have a higher capacity to acidify extracellular milieu by a ductal mechanism. Clin Exp Metastasis. 15:382–392. 1997. View Article : Google Scholar : PubMed/NCBI
28	Ohta T, Numata M, Yagishita H, et al: Expression of 16 kDa proteolipid of vacuolar-type H(+)-ATPase in human pancreatic cancer. Br J Cancer. 73:1511–1517. 1996.
29	Donald WE and Walter HS: The pH of inflammatory exudates. Proc Soc Exp Biol Med. 137:1328–1332. 1971. View Article : Google Scholar
30	Simmen HP, Battaglia H, Giovanoli P, et al: Analysis of pH, pO₂ and pCO₂ in drainage fluid allows for rapid detection of infectious complications during the follow-up period after abdominal surgery. Infection. 22:386–389. 1994.PubMed/NCBI
31	Ward TT and Steigbigel RT: Acidosis of synovial fluid correlates with synovial fluid leukocytosis. Am J Med. 64:933–936. 1978. View Article : Google Scholar : PubMed/NCBI
32	Wintroub BU, Klickstein LB and Watt KW: A human neutrophil-dependent pathway for generation of angiotensin II. Purification of the product and identification as angiotensin II. J Clin Invest. 68:484–490. 1981. View Article : Google Scholar : PubMed/NCBI
33	Rykl J, Thiemann J, Kuzawski S, et al: Renal cathepsin G and angiotensin II generation. J Hypertens. 24:1797–1807. 2006. View Article : Google Scholar : PubMed/NCBI
34	Kawabata K, Hagio T, Matsumoto S, et al: Delayed neutrophil elastase inhibition prevents subsequent progression of acute lung injury induced by endotoxin inhalation in hamsters. Am J Respir Crit Care Med. 161:2013–2018. 2000. View Article : Google Scholar : PubMed/NCBI
35	Young RE, Voisin MB, Wang S, et al: Role of neutrophil elastase in LTB4-induced neutrophil transmigration in vivo assessed with a specific inhibitor and neutrophil elastase deficient mice. Br J Pharmacol. 151:628–637. 2007. View Article : Google Scholar : PubMed/NCBI