A 60 kDa prolactin variant secreted by cervical cancer cells modulates apoptosis and cytokine production
- Authors:
- Adrián Ramírez De Arellano
- Annie Riera Leal
- Edgar I. Lopez-Pulido
- Luis Renee González-Lucano
- José Macías Barragan
- Susana Del Toro Arreola
- Mariel García-Chagollan
- Claudia A. Palafox-Sánchez
- José F. Muñoz-Valle
- Ana Laura Pereira-Suárez
-
Affiliations: Doctorate Program in Biomedical Sciences, University Center for Health Sciences, University of Guadalajara, Guadalajara, Jalisco, Mexico, Department of Clinics, University Center of Los Altos, Tepatitlan de Morelos, University of Guadalajara, Guadalajara, Jalisco, Mexico, Institute of Technology and Higher Education of Monterrey, Campus Guadalajara, Zapopan, Jalisco, Mexico, Department of Health Sciences, University Center of Los Valles, University of Guadalajara, Ameca, Jalisco, Mexico, Department of Physiology, University Center for Health Sciences, University of Guadalajara, Guadalajara, Jalisco, Mexico, Research Institute in Biomedical Sciences, University Center for Health Sciences, University of Guadalajara, Guadalajara, Jalisco, Mexico - Published online on: January 19, 2018 https://doi.org/10.3892/or.2018.6222
- Pages: 1253-1260
This article is mentioned in:
Abstract
Goffin V, Binart N, Touraine P and Kelly PA: Prolactin: The new biology of an old hormone. Annu Rev Physiol. 64:47–67. 2002. View Article : Google Scholar : PubMed/NCBI | |
Reber PM: Prolactin and immunomodulation. Am J Med. 95:637–644. 1993. View Article : Google Scholar : PubMed/NCBI | |
Freeman ME, Kanyicska B, Lerant A and Nagy G: Prolactin: Structure, function, and regulation of secretion. Physiol Rev. 80:1523–631. 2000. View Article : Google Scholar : PubMed/NCBI | |
Athreya BH, Pletcher J, Zulian F, Weiner DB and Williams WV: Subset-specific effects of sex hormones and pituitary gonadotropins on human lymphocyte proliferation in vitro. Clin Immunol Immunopathol. 66:201–211. 1993. View Article : Google Scholar : PubMed/NCBI | |
Matera L, Mori M and Galetto A: Galetto, Effect of prolactin on the antigen presenting function of monocyte-derived dendritic cells. Lupus. 10:728–734. 2001. View Article : Google Scholar : PubMed/NCBI | |
Lahat N, Miller A, Shtiller R and Touby E: Differential effects of prolactin upon activation and differentiation of human B lymphocytes. J Neuroimmunol. 47:35–40. 1993. View Article : Google Scholar : PubMed/NCBI | |
Ben-Jonathan N, Mershon JL, Allen DL and Steinmetz RW: Extrapituitary prolactin: Distribution, regulation, functions, and clinical aspects. Endocr Rev. 17:639–669. 1996. View Article : Google Scholar : PubMed/NCBI | |
De Bellis A, Bizzarro A, Pivonello R, Lombardi G and Bellastella A: Prolactin and autoimmunity. Pituitary. 8:25–30. 2005. View Article : Google Scholar : PubMed/NCBI | |
Sodhi A and Tripathi A: Prolactin and growth hormone induce differential cytokine and chemokine profile in murine peritoneal macrophages in vitro: Involvement of p-38 MAP kinase, STAT3 and NF-kappaB. Cytokine. 41:162–173. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tripathi A and Sodhi A: Prolactin-induced production of cytokines in macrophages in vitro involves JAK/STAT and JNK MAPK pathways. Int Immunol. 20:327–336. 2008. View Article : Google Scholar : PubMed/NCBI | |
Corbacho AM, Macotela Y, Nava G, Eiserich JP, Cross CE, Martínez de la Escalera G and Clapp C: Cytokine induction of prolactin receptors mediates prolactin inhibition of nitric oxide synthesis in pulmonary fibroblasts. FEBS Lett. 544:171–175. 2003. View Article : Google Scholar : PubMed/NCBI | |
Jara LJ, Vera-Lastra O, Miranda JM, Alcala M and Alvarez-Nemegyei J: Prolactin in human systemic lupus erythematosus. Lupus. 10:748–756. 2001. View Article : Google Scholar : PubMed/NCBI | |
Chikanza IC, Petrou P, Chrousos G, Kingsley G and Panayi GS: Excessive and dysregulated secretion of prolactin in rheumatoid arthritis: Immunopathogenetic and therapeutic implications. Br J Rheumatol. 32:445–448. 1993. View Article : Google Scholar : PubMed/NCBI | |
El Miedany YM, Ahmed I, Moustafa H and El Baddini M: Hyperprolactinemia in Sjogren's syndrome: A patient subset or a disease manifestation? Joint Bone Spine. 71:203–208. 2004. View Article : Google Scholar : PubMed/NCBI | |
Chikanza IC: Prolactin and neuroimmunomodulation: in vitro and in vivo observations. Ann NY Acad Sci. 876:119–130. 1999. View Article : Google Scholar : PubMed/NCBI | |
Nicoletti F, Di Marco R, Barcellini W, Magro G, Schorlemmer HU, Kurrle R, Lunetta M, Grasso S, Zaccone P and Meroni P: Protection from experimental autoimmune diabetes in the non-obese diabetic mouse with soluble interleukin-1 receptor. Eur J Immunol. 24:1843–1847. 1994. View Article : Google Scholar : PubMed/NCBI | |
Nicoletti F, Zaccone P, Di Marco R, Lunetta M, Magro G, Grasso S, Meroni P and Garotta G: Prevention of spontaneous autoimmune diabetes in diabetes-prone BB rats by prophylactic treatment with antirat interferon-gamma antibody. Endocrinology. 138:281–288. 1997. View Article : Google Scholar : PubMed/NCBI | |
Joosten LA, Helsen MM, van de Loo FA and van den Berg WB: Anticytokine treatment of established type II collagen-induced arthritis in DBA/1 mice: A comparative study using anti-TNFalpha, anti-IL-1alpha/beta and IL-1Ra. Arthritis Rheum. 58:S110–S122. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sinha YN: Structural variants of prolactin: Occurrence and physiological significance. Endocr Rev. 16:354–369. 1995. View Article : Google Scholar : PubMed/NCBI | |
Sinha YN: Prolactin variants. Trends Endocrinol Metab. 3:100–106. 1992. View Article : Google Scholar : PubMed/NCBI | |
Champier J, Claustrat B, Sassolas G and Berger M: Detection and enzymatic deglycosylation of a glycosylated variant of prolactin in human plasma. FEBS Lett. 212:220–224. 1987. View Article : Google Scholar : PubMed/NCBI | |
González-Lucano LR, Muñoz-Valle JF, Ascencio-Cedillo R, Domínguez-Rosales JA, López-Rincón G, Del Toro-Arreola S, Bueno-Topete M, Daneri-Navarro A, Estrada-Chávez C and Pereira-Suárez AL: Increased expression of the prolactin receptor is associated with malignant laryngeal tumors. Exp Ther Med. 3:603–607. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lopez-Pulido EI, Muñoz-Valle JF, Del Toro-Arreola S, Jave-Suárez LF, Bueno-Topete MR, Estrada-Chávez C and Pereira-Suárez AL: High expression of prolactin receptor is associated with cell survival in cervical cancer cells. Cancer Cell Int. 13:1032013. View Article : Google Scholar : PubMed/NCBI | |
López-Rincón G, Pereira-Suárez AL, Del Toro-Arreola S, Sánchez-Hernández PE, Ochoa-Zarzosa A, Muñoz-Valle JF and Estrada-Chávez C: Lipopolysaccharide induces the expression of an autocrine prolactin loop enhancing inflammatory response in monocytes. J Inflamm. 10:242013. View Article : Google Scholar | |
Larrea F, Martínez-Castillo A, Cabrera V, Alcocer-Varela J, Queipo G, Cariño C and Alarcón-Segovia D: A bioactive 60-kilodalton prolactin species is preferentially secreted in cultures of mitogen-stimulated and nonstimulated peripheral blood mononuclear cells from subjects with systemic lupus erythematosus. J Clin Endocrinol Metab. 82:3664–3669. 1997. View Article : Google Scholar : PubMed/NCBI | |
Goffin V, Binart N, Clément-Lacroix P, Bouchard B, Bole-Feysot C, Edery M, Lucas BK, Touraine P, Pezet A, Maaskant R, et al: From the molecular biology of prolactin and its receptor to the lessons learned from knockout mice models. Genet Anal. 15:189–201. 1999. View Article : Google Scholar : PubMed/NCBI | |
Schindler C: Cytokines and JAK-STAT signaling. Exp Cell Res. 253:7–14. 1999. View Article : Google Scholar : PubMed/NCBI | |
Das R and Vonderhaar BK: Involvement of SHC, GRB2, SOS and RAS in prolactin signal transduction in mammary epithelial cells. Oncogene. 13:1139–1145. 1996.PubMed/NCBI | |
Domínguez-Cáceres MA, García-Martínez JM, Calcabrini A, González L, Porque PG, León J and Martín-Pérez J: Prolactin induces c-Myc expression and cell survival through activation of Src/Akt pathway in lymphoid cells. Oncogene. 23:7378–7390. 2004. View Article : Google Scholar : PubMed/NCBI | |
Berlanga JJ, Gualillo O, Buteau H, Applanat M, Kelly PA and Edery M: Prolactin activates tyrosyl phosphorylation of insulin receptor substrate 1 and phosphatidylinositol-3-OH kinase. J Biol Chem. 272:2050–2052. 1997. View Article : Google Scholar : PubMed/NCBI | |
Ramírez de Arellano A, Lopez-Pulido EI, Martínez-Neri PA, Estrada Chávez C, González Lucano R, Fafutis-Morris M, Aguilar-Lemarroy A, Muñoz-Valle JF and Pereira-Suárez AL: STAT3 activation is required for the antiapoptotic effects of prolactin in cervical cancer cells. Cancer Cell Int. 15:832015. View Article : Google Scholar : PubMed/NCBI | |
López-Rincón G, Mancilla R, Pereira-Suárez AL, Martínez-Neri PA, Ochoa-Zarzosa A, Muñoz-Valle JF and Estrada-Chávez C: Expression of autocrine prolactin and the short isoform of prolactin receptor are associated with inflammatory response and apoptosis in monocytes stimulated with Mycobacterium bovis proteins. Exp Mol Pathol. 98:517–526. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yonezawa T, Chen KH, Ghosh MK, Rivera L, Dill R, Ma L, Villa PA, Kawaminami M and Walker AM: Anti-metastatic outcome of isoform-specific prolactin receptor targeting in breast cancer. Cancer Lett. 366:84–92. 2015. View Article : Google Scholar : PubMed/NCBI | |
Neradugomma NK, Subramaniam D, Tawfsik OW, Goffin V, Kumar TR, Jensen RA and Anant S: Prolactin signaling enhances colon cancer stemness by modulating Notch signaling in a Jak2-STAT3/ERK manner. Carcinogenesis. 35:795–806. 2014. View Article : Google Scholar : PubMed/NCBI | |
Goffin V, Hoang DT, Bogorad RL and Nevalainen MT: Prolactin regulation of the prostate gland: A female player in a male game. Nat Rev Urol. 8:597–607. 2011. View Article : Google Scholar : PubMed/NCBI | |
Robertson FG, Harris J, Naylor MJ, Oakes SR, Kindblom J, Dillner K, Wennbo H, Törnell J, Kelly PA, Green J and Ormandy CJ: Prostate development and carcinogenesis in prolactin receptor knockout mice. Endocrinology. 144:3196–3205. 2003. View Article : Google Scholar : PubMed/NCBI | |
Clevenger CV, Furth PA, Hankinson SE and Schuler LA: The role of prolactin in mammary carcinoma. Endocr Rev. 24:1–27. 2003. View Article : Google Scholar : PubMed/NCBI | |
Tworoger SS and Hankinson SE: Prolactin and breast cancer etiology: An epidemiologic perspective. J Mammary Gland Biol Neoplasia. 13:41–53. 2008. View Article : Google Scholar : PubMed/NCBI | |
Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ascencio-Cedillo R, López-Pulido EI, Muñoz-Valle JF, Villegas-Sepúlveda N, Del Toro-Arreola S, Estrada-Chávez C, Daneri-Navarro A, Franco-Topete R, Pérez-Montiel D, García-Carrancá A and Pereira-Suárez AL: Prolactin and prolactin receptor expression in cervical intraepithelial neoplasia and cancer. Pathol Oncol Res. 21:241–246. 2014. View Article : Google Scholar : PubMed/NCBI | |
Gout PW, Beer CT and Noble RL: Prolactin-stimulated growth of cell cultures established from malignant Nb rat lymphomas. Cancer Res. 40:2433–2436. 1980.PubMed/NCBI | |
Noble RL, Beer CT and Gout PW: Evidence in vivo and in vitro of a role for the pituitary in the growth of malignant lymphomas in Nb rats. Cancer Res. 40:2437–2440. 1980.PubMed/NCBI | |
Perks CM, Keith AJ, Goodhew KL, Savage PB, Winters ZE and Holly JM: Prolactin acts as a potent survival factor for human breast cancer cell lines. Br J Cancer. 91:305–311. 2004. View Article : Google Scholar : PubMed/NCBI | |
Giuffrida D, Perdichizzi A, Giuffrida MC, La Vignera S, D'Agata R, Vicari E and Calogero AE: Does prolactin induce apoptosis? Evidences in a prostate cancer in vitro model. J Endocrinol Invest. 33:313–317. 2010. View Article : Google Scholar : PubMed/NCBI | |
Asai-Sato M, Nagashima Y, Miyagi E, Sato K, Ohta I, Vonderhaar BK and Hirahara F: Prolactin inhibits apoptosis of ovarian carcinoma cells induced by serum starvation or cisplatin treatment. Int J Cancer. 115:539–544. 2005. View Article : Google Scholar : PubMed/NCBI | |
Shoupe D, Montz FJ, Kletzky OA and DiZerega GS: Prolactin molecular heterogeneity. Response to thyrotropin-releasing hormone stimulation of concanavalin A-bound and -unbound immunoassayable prolactin during human pregnancy. Am J Obstet Gynecol. 147:482–487. 1983. View Article : Google Scholar : PubMed/NCBI | |
Qin HR, Kim HJ, Kim JY, Hurt EM, Klarmann GJ, Kawasaki BT, Duhagon Serrat MA and Farrar WL: Activation of signal transducer and activator of transcription 3 through a phosphomimetic serine 727 promotes prostate tumorigenesis independent of tyrosine 705 phosphorylation. Cancer Res. 68:7736–7741. 2008. View Article : Google Scholar : PubMed/NCBI | |
Clevenger CV: Roles and regulation of stat family transcription factors in human breast cancer. Am J Pathol. 165:1449–1460. 2004. View Article : Google Scholar : PubMed/NCBI | |
Ling X and Arlinghaus RB: Knockdown of STAT3 expression by RNA interference inhibits the induction of breast tumors in immunocompetent mice. Cancer Res. 65:2532–2536. 2005. View Article : Google Scholar : PubMed/NCBI | |
Chan KS, Sano S, Kiguchi K, Anders J, Komazawa N, Takeda J and DiGiovanni J: Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis. J Clin Invest. 114:720–728. 2004. View Article : Google Scholar : PubMed/NCBI | |
Pedranzini L, Leitch A and Bromberg J: Stat3 is required for the development of skin cancer. J Clin Invest. 114:619–622. 2004. View Article : Google Scholar : PubMed/NCBI | |
Alvarez JV, Mukherjee N, Chakravarti A, Robe P, Zhai G, Chakladar A, Loeffler J, Black P and Frank DA: A STAT3 gene expression signature in gliomas is associated with a poor prognosis. Transl Oncogenomics. 2:99–105. 2007.PubMed/NCBI | |
Abou-Ghazal M, Yang DS, Qiao W, Reina-Ortiz C, Wei J, Kong LY, Fuller GN, Hiraoka N, Priebe W, Sawaya R and Heimberger AB: The incidence, correlation with tumor-infiltrating inflammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clin Cancer Res. 14:8228–8235. 2008. View Article : Google Scholar : PubMed/NCBI | |
Shukla S, Mahata S, Shishodia G, Pandey A, Tyagi A, Vishnoi K, Basir SF, Das BC and Bharti AC: Functional regulatory role of STAT3 in HPV16-mediated cervical carcinogenesis. PLoS One. 8:e678492013. View Article : Google Scholar : PubMed/NCBI | |
Zhang Z, Mao H, Du X, Zhu J, Xu Y, Wang S, Xu X, Ji P, Yu Y, Cao B, et al: A novel small molecule agent displays potent anti-myeloma activity by inhibiting the JAK2-STAT3 signaling pathway. Oncotarget. 7:9296–9308. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wang S, An W, Yao Y, Chen R, Zheng X, Yang W, Zhao Y, Hu X, Jiang E, Bie Y, et al: Interleukin 37 expression inhibits STAT3 to suppress the proliferation and invasion of human cervical cancer cells. J Cancer. 6:962–969. 2015. View Article : Google Scholar : PubMed/NCBI | |
Eichhorn JM, Alford SE, Sakurikar N and Chambers TC: Molecular analysis of functional redundancy among anti-apoptotic Bcl-2 proteins and its role in cancer cell survival. Exp Cell Res. 322:415–424. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chao DT, Linette GP, Boise LH, White LS, Thompson CB and Korsmeyer SJ: Bcl-XL and Bcl-2 repress a common pathway of cell death. J Exp Med. 182:821–828. 1995. View Article : Google Scholar : PubMed/NCBI | |
Villunger A, Scott C, Bouillet P and Strasser A: Essential role for the BH3-only protein Bim but redundant roles for Bax, Bcl-2, and Bcl-w in the control of granulocyte survival. Blood. 101:2393–2400. 2003. View Article : Google Scholar : PubMed/NCBI | |
Paradkar PH, Joshi JV, Mertia PN, Agashe SV and Vaidya RA: Role of cytokines in genesis, progression and prognosis of cervical cancer. Asian Pac J Cancer Prev. 15:3851–3864. 2014. View Article : Google Scholar : PubMed/NCBI | |
Goncalves MA and Donadi EA: Immune cellular response to HPV: Current concepts. Braz J Infect Dis. 8:1–9. 2004. View Article : Google Scholar : PubMed/NCBI |