AT1 receptor blockade delays postlactational mammary gland involution: A novel role for the renin angiotensin system

FASEB Journal

Volumn 26, Issue 5, 2012, Pages 1982-1994

  Nahmod, Karen A ^a   Walther, Thomas ^b,c   Cambados, Nadia ^d   Fernandez, Natalia ^d   Meiss, Roberto ^a   Tappenbeck, Nils ^b,c   Wang, Yong ^b,c   Raffo, Diego ^e   Simian, Marina ^e   Schwiebs, Anja ^b,c   Pozner, Roberto G ^a   Fuxman Bass, Juan I ^a   Pozzi, Andrea G ^d   Geffner, Jorge R ^a   Kordon, Edith C ^d   Schere Levy, Carolina ^d  

^a ACADEMIA NACIONAL DE MEDICINA   (Argentina)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF HULL   (United Kingdom)

^d Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^e UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

AKT; Angiotensin II; Apoptosis; Metalloproteases; STAT3

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 1A RECEPTOR; ANGIOTENSIN 1B RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; ANGIOTENSINOGEN; BETA ACTIN; BETA TUBULIN; COLLAGEN; DIPEPTIDYL CARBOXYPEPTIDASE; GELATINASE A; GELATINASE B; I KAPPA B ALPHA; IRBESARTAN; LEUKEMIA INHIBITORY FACTOR; LOSARTAN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BCL XL; PROTEIN KINASE B; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; ANGIOTENSIN 1 RECEPTOR ANTAGONIST;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CELL GROWTH; CELL INVASION; CELL TYPE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; INVOLUTION; LACTATION; MAMMARY GLAND; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BLOCKING; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SIGNAL TRANSDUCTION; WEANING; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; DOSE RESPONSE; DRUG EFFECT; METABOLISM; NICK END LABELING; PHYSIOLOGY; POLYMERASE CHAIN REACTION; UDDER;

ANIMALIA; MUS;

ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; APOPTOSIS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; IN SITU NICK-END LABELING; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED BALB C; POLYMERASE CHAIN REACTION; RECEPTOR, ANGIOTENSIN, TYPE 1; RENIN-ANGIOTENSIN SYSTEM; SIGNAL TRANSDUCTION;

EID: 84860897119     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-191932     Document Type: Article

References (58)

1. Nahmod, V. E., Finkielman, S., Benarroch, E. E., and Pirola, C. J. (1978) Angiotensin regulates release and synthesis of serotonin in brain. Science 202, 1091-1093
2. Phillips, M. I., Speakman, E. A., and Kimura, B. (1993) Levels of angiotensin and molecular biology of the tissue renin angiotensin systems. Regul. Pept. 43, 1-20
3. Zhuo, J., Moeller, I., Jenkins, T., Chai, S. Y., Allen, A. M., Ohishi, M., and Mendelsohn, F. A. (1998) Mapping tissue angiotensinconverting enzyme and angiotensin AT1, AT2 and AT4 receptors. J. Hypertens. 16, 2027-2037 (Pubitemid 29002384)
4. Silver, R. B., Reid, A. C., Mackins, C. J., Askwith, T., Schaefer, U., Herzlinger, D., and Levi, R. (2004) Mast cells: a unique source of renin. Proc. Natl. Acad. Sci. U. S. A. 101, 13607-13612 (Pubitemid 39238450)
5. Sadoshima, J. (2000) Cytokine actions of angiotensin II. Circ. Res. 86, 1187-1189
6. Diep, Q. N., El Mabrouk, M., Touyz, R. M., and Schiffrin, E. L. (2001) Expression of cell cycle proteins in blood vessels of angiotensin II-infused rats: role of AT(1) receptors. Hypertension 37, 604-608 (Pubitemid 32199035)
7. Phillips, M. I., and Kagiyama, S. (2002) Angiotensin II as a pro-inflammatory mediator. Curr. Opin. Investig. Drugs 3, 569-577
8. Clauser, E., Curnow, K. M., Davies, E., Conchon, S., Teutsch, B., Vianello, B., Monnot, C., and Corvol, P. (1996) Angiotensin II receptors: protein and gene structures, expression and potential pathological involvements. Eur. J. Endocrinol. 134, 403-411 (Pubitemid 26155496)
9. Burson, J. M., Aguilera, G., Gross, K. W., and Sigmund, C. D. (1994) Differential expression of angiotensin receptor 1A and 1B in mouse. Am. J. Physiol. 267, E260-267
10. Unger, T. (2002) The role of the renin-angiotensin system in the development of cardiovascular disease. Am. J. Cardiol. 89, 3A-9A; discussion 10A
11. Sutherland, K. D., Lindeman, G. J., and Visvader, J. E. (2007) The molecular culprits underlying precocious mammary gland involution. J. Mammary Gland Biol. Neoplasia 12, 15-23 (Pubitemid 46394922)
12. Chapman, R. S., Lourenco, P. C., Tonner, E., Flint, D. J., Selbert, S., Takeda, K., Akira, S., Clarke, A. R., and Watson, C. J. (1999) Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3. Genes Dev. 13, 2604-2616 (Pubitemid 29489651)
13. Kritikou, E. A., Sharkey, A., Abell, K., Came, P. J., Anderson, E., Clarkson, R. W., and Watson, C. J. (2003) A dual, non-redundant, role for LIF as a regulator of development and STAT3-mediated cell death in mammary gland. Development 130, 3459-3468 (Pubitemid 37010009)
14. Schere-Levy, C., Buggiano, V., Quaglino, A., Gattelli, A., Cirio, M. C., Piazzon, I., Vanzulli, S., and Kordon, E. C. (2003) Leukemia inhibitory factor induces apoptosis of the mammary epithelial cells and participates in mouse mammary gland involution. Exp. Cell Res. 282, 35-47 (Pubitemid 36062610)
15. Talhouk, R. S., Chin, J. R., Unemori, E. N., Werb, Z., and Bissell, M. J. (1991) Proteinases of the mammary gland: developmental regulation in vivo and vectorial secretion in culture. Development 112, 439-449
16. Schorr, K., Li, M., Bar-Peled, U., Lewis, A., Heredia, A., Lewis, B., Knudson, C. M., Korsmeyer, S. J., Jager, R., Weiher, H., and Furth, P. A. (1999) Gain of Bcl-2 is more potent than bax loss in regulating mammary epithelial cell survival in vivo. Cancer Res. 59, 2541-2545 (Pubitemid 29269094)
17. Walton, K. D., Wagner, K. U., Rucker, E. B., 3rd, Shillingford, J. M., Miyoshi, K., and Hennighausen, L. (2001) Conditional deletion of the bcl-x gene from mouse mammary epithelium results in accelerated apoptosis during involution but does not compromise cell function during lactation. Mech. Dev. 109, 281-293 (Pubitemid 33112039)
18. Schwertfeger, K. L., Richert, M. M., and Anderson, S. M. (2001) Mammary gland involution is delayed by activated Akt in transgenic mice. Mol. Endocrinol. 15, 867-881 (Pubitemid 32510636)
19. Inwang, E. R., Puddefoot, J. R., Brown, C. L., Goode, A. W., Marsigliante, S., Ho, M. M., Payne, J. G., and Vinson, G. P. (1997) Angiotensin II type 1 receptor expression in human breast tissues. Br. J. Cancer 75, 1279-1283 (Pubitemid 27179816)
20. Tahmasebi, M., Barker, S., Puddefoot, J. R., and Vinson, G. P. (2006) Localisation of renin-angiotensin system (RAS) components in breast. Br. J. Cancer 95, 67-74 (Pubitemid 43980556)
21. De Paepe, B., Verstraeten, V. L., De Potter, C. R., Vakaet, L. A., and Bullock, G. R. (2001) Growth stimulatory angiotensin II type-1 receptor is upregulated in breast hyperplasia and in situ carcinoma but not in invasive carcinoma. Histochem. Cell Biol. 116, 247-254 (Pubitemid 32930137)
22. Herr, D., Rodewald, M., Fraser, H. M., Hack, G., Konrad, R., Kreienberg, R., and Wulff, C. (2008) Potential role of reninangiotensin-system for tumor angiogenesis in receptor negative breast cancer. Gynecol. Oncol. 109, 418-425
23. Kodama, H., Fukuda, K., Pan, J., Makino, S., Sano, M., Takahashi, T., Hori, S., and Ogawa, S. (1998) Biphasic activation of the JAK/STAT pathway by angiotensin II in rat cardiomyocytes. Circ. Res. 82, 244-250 (Pubitemid 28080107)
24. Eguchi, S., Dempsey, P. J., Frank, G. D., Motley, E. D., and Inagami, T. (2001) Activation of MAPKs by angiotensin II in vascular smooth muscle cells. Metalloprotease-dependent EGF receptor activation is required for activation of ERK and p38 MAPK but not for JNK. J. Biol. Chem. 276, 7957-7962
25. Browatzki, M., Larsen, D., Pfeiffer, C. A., Gehrke, S. G., Schmidt, J., Kranzhofer, A., Katus, H. A., and Kranzhofer, R. (2005) Angiotensin II stimulates matrix metalloproteinase secretion in human vascular smooth muscle cells via NF-κB and activator protein 1 in a redox-sensitive manner. J. Vasc. Res. 42, 415- 423
26. Zhang, L., Ma, Y., Zhang, J., Cheng, J., and Du, J. (2005) A new cellular signaling mechanism for angiotensin II activation of NF-κB: An IκB-independent, RSK-mediated phosphorylation of p65. Arterioscler. Thromb. Vasc. Biol. 25, 1148-1153 (Pubitemid 40776601)
27. Mehta, P. K., and Griendling, K. K. (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am. J. Physiol. Cell Physiol. 292, C82-C97 (Pubitemid 46127306)
28. Zhao, Y., Chen, X., Cai, L., Yang, Y., Sui, G., and Fu, S. (2010) Angiotensin II/angiotensin II type I receptor (AT1R) signaling promotes MCF-7 breast cancer cells survival via PI3-kinase/Akt pathway. J. Cell. Physiol. 225, 168-173
29. Quaglino, A., Salierno, M., Pellegrotti, J., Rubinstein, N., and Kordon, E. C. (2009) Mechanical strain induces involution-associated events in mammary epithelial cells. BMC Cell Biol. 10, 55
30. Oliverio, M. I., Kim, H. S., Ito, M., Le, T., Audoly, L., Best, C. F., Hiller, S., Kluckman, K., Maeda, N., Smithies, O., and Coffman, T. M. (1998) Reduced growth, abnormal kidney structure, and type 2 (AT2) angiotensin receptor-mediated blood pressure regulation in mice lacking both AT1A and AT1B receptors for angiotensin II. Proc. Natl. Acad. Sci. U. S. A. 95, 15496 -15501
31. Wang, J. M., Tan, J., and Leenen, F. H. (2003) Central nervous system blockade by peripheral administration of AT1 receptor blockers. J. Cardiovasc. Pharmacol. 41, 593-599 (Pubitemid 36373797)
32. Gembardt, F., Heringer-Walther, S., van Esch, J. H., Sterner-Kock, A., van Veghel, R., Le, T. H., Garrelds, I. M., Coffman, T. M., Danser, A. H., Schultheiss, H. P., and Walther, T. (2008) Cardiovascular phenotype of mice lacking all three subtypes of angiotensin II receptors. FASEB J. 22, 3068-3077
33. Levy, C. S., Slomiansky, V., Gattelli, A., Nahmod, K., Pelisch, F., Blaustein, M., Srebrow, A., Coso, O. A., and Kordon, E. C. (2010) Tumor necrosis factor alpha induces LIF expression through ERK1/2 activation in mammary epithelial cells. J. Cell. Biochem. 110, 857-865
34. Gross, V., Schunck, W. H., Honeck, H., Milia, A. F., Kargel, E., Walther, T., Bader, M., Inagami, T., Schneider, W., and Luft, F. C. (2000) Inhibition of pressure natriuresis in mice lacking the AT2 receptor. Kidney Int. 57, 191-202 (Pubitemid 30227766)
35. Gembardt, F., Sterner-Kock, A., Imboden, H., Spalteholz, M., Reibitz, F., Schultheiss, H. P., Siems, W. E., and Walther, T. (2005) Organ-specific distribution of ACE2 mRNA and correlating peptidase activity in rodents. Peptides 26, 1270 -1277
36. Lund, L. R., Romer, J., Thomasset, N., Solberg, H., Pyke, C., Bissell, M. J., Dano, K., and Werb, Z. (1996) Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development 122, 181-193 (Pubitemid 26038430)
37. Roks, A. J., and Henning, R. H. (2003) Angiotensin peptides: ready to re(de)fine the angiotensin system? J. Hypertens. 21, 1269-1271
38. Vinson, G. P., Ho, M. M., and Puddefoot, J. R. (1995) The distribution of angiotensin II type 1 receptors, and the tissue renin-angiotensin systems. Mol. Med. Today. 1, 35-39
39. Tybitanclova, K., Macejova, D., Liska, J., Brtko, J., and Zorad, S. (2005) AT1 receptor and ACE mRNA are increased in chemically induced carcinoma of rat mammary gland. Mol. Cell. Endocrinol. 244, 42-46 (Pubitemid 41628227)
40. Kosugi, M., Miyajima, A., Kikuchi, E., Horiguchi, Y., and Murai, M. (2006) Angiotensin II type 1 receptor antagonist candesartan as an angiogenic inhibitor in a xenograft model of bladder cancer. Clin. Cancer Res. 12, 2888-2893
41. Rhodes, D. R., Ateeq, B., Cao, Q., Tomlins, S. A., Mehra, R., Laxman, B., Kalyana-Sundaram, S., Lonigro, R. J., Helgeson, B. E., Bhojani, M. S., Rehemtulla, A., Kleer, C. G., Hayes, D. F., Lucas, P. C., Varambally, S., and Chinnaiyan, A. M. (2009) AGTR1 overexpression defines a subset of breast cancer and confers sensitivity to losartan, an AGTR1 antagonist. Proc. Natl. Acad. Sci. U. S. A. 106, 10284-10289
42. Diop-Frimpong, B., Chauhan, V. P., Krane, S., Boucher, Y., and Jain, R. K. (2011) Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors. Proc. Natl. Acad. Sci. U. S. A. 108, 2909-2914
43. Baxter, F. O., Came, P. J., Abell, K., Kedjouar, B., Huth, M., Rajewsky, K., Pasparakis, M., and Watson, C. J. (2006) IKK/2 induces TWEAK and apoptosis in mammary epithelial cells. Development 133, 3485-3494 (Pubitemid 44501850)
44. Watson, C. J. (2006) Post-lactational mammary gland regression: molecular basis and implications for breast cancer. Expert Rev. Mol. Med. 8, 1-15
45. Rahman, M., Kimura, S., Nishiyama, A., Hitomi, H., Zhang, G., and Abe, Y. (2004) Angiotensin II stimulates superoxide production via both angiotensin AT1A and AT1B receptors in mouse aorta and heart. Eur. J. Pharmacol. 485, 243-249 (Pubitemid 38134421)
46. Zhou, Y., Dirksen, W. P., Chen, Y., Morris, M., Zweier, J. L., and Periasamy, M. (2005) A major role for AT1b receptor in mouse mesenteric resistance vessels and its distribution in heart and neuroendocrine tissues. J. Mol. Cell. Cardiol. 38, 693-696 (Pubitemid 40461833)
47. Zhao, L., Melenhorst, J. J., and Hennighausen, L. (2002) Loss of interleukin 6 results in delayed mammary gland involution: a possible role for mitogen-activated protein kinase and not signal transducer and activator of transcription 3. Mol. Endocrinol. 16, 2902-2912 (Pubitemid 36024180)
48. Pan, J., Fukuda, K., Saito, M., Matsuzaki, J., Kodama, H., Sano, M., Takahashi, T., Kato, T., and Ogawa, S. (1999) Mechanical stretch activates the JAK/STAT pathway in rat cardiomyocytes. Circ. Res. 84, 1127-1136 (Pubitemid 29244774)
49. Zampetaki, A., Zhang, Z., Hu, Y., and Xu, Q. (2005) Biomechanical stress induces IL-6 expression in smooth muscle cells via Ras/Rac1-p38 MAPK-NF-κB signaling pathways. Am. J. Physiol. Heart Circ. Physiol. 288, H2946-H2954 (Pubitemid 40720679)
50. Sadoshima, J., Xu, Y., Slayter, H. S., and Izumo, S. (1993) Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell 75, 977-984 (Pubitemid 24014554)
51. Kojima, M., Shiojima, I., Yamazaki, T., Komuro, I., Zou, Z., Wang, Y., Mizuno, T., Ueki, K., Tobe, K., Kadowaki, T. (1994) Angiotensin II receptor antagonist TCV-116 induces regression of hypertensive left ventricular hypertrophy in vivo and inhibits the intracellular signaling pathway of stretch-mediated cardiomyocyte hypertrophy in vitro. Circulation 89, 2204 -2211
52. Yamazaki, T., Komuro, I., Kudoh, S., Zou, Y., Shiojima, I., Mizuno, T., Takano, H., Hiroi, Y., Ueki, K., Tobe, K., Kadowaki, T., Nagai, R., Yazaki, Y. (1995) Angiotensin II partly mediates mechanical stressinduced cardiac hypertrophy. Circ. Res. 77, 258-265
53. Zou, Y., Akazawa, H., Qin, Y., Sano, M., Takano, H., Minamino, T., Makita, N., Iwanaga, K., Zhu, W., Kudoh, S., Toko, H., Tamura, K., Kihara, M., Nagai, T., Fukamizu, A., Umemura, S., Iiri, T., Fujita, T., and Komuro, I. (2004) Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat. Cell Biol. 6, 499-506 (Pubitemid 38786592)
54. Luchtefeld, M., Grote, K., Grothusen, C., Bley, S., Bandlow, N., Selle, T., Struber, M., Haverich, A., Bavendiek, U., Drexler, H., and Schieffer, B. (2005) Angiotensin II induces MMP-2 in a p47phox-dependent manner. Biochem. Biophys. Res. Commun. 328, 183-188 (Pubitemid 40164653)
55. Guo, R. W., Yang, L. X., Wang, H., Liu, B., and Wang, L. (2008) Angiotensin II induces matrix metalloproteinase-9 expression via a nuclear factor-κB-dependent pathway in vascular smooth muscle cells. Regul. Pept. 147, 37-44
56. Ibanez, P., Solis, N., Pizarro, M., Aguayo, G., Duarte, I., Miquel, J. F., Accatino, L., and Arrese, M. (2007) Effect of losartan on early liver fibrosis development in a rat model of nonalcoholic steatohepatitis. J. Gastroenterol. Hepatol. 22, 846-851 (Pubitemid 46911021)
57. Yvan-Charvet, L., and Quignard-Boulange, A. (2011) Role of adipose tissue renin-angiotensin system in metabolic and inflammatory diseases associated with obesity. Kidney Int. 79, 162-168
58. Crandall, D. L., Armellino, D. C., Busler, D. E., McHendry-Rinde, B., and Kral, J. G. (1999) Angiotensin II receptors in human preadipocytes: role in cell cycle regulation. Endocrinology 140, 154-158 (Pubitemid 29011154)