Epicardial-derived adrenomedullin drives cardiac hyperplasia during embryogenesis

Developmental Dynamics

Volumn 243, Issue 2, 2014, Pages 243-256

  Wetzel Strong, Sarah E ^a   Li, Manyu ^a   Klein, Klara R ^a   Nishikimi, Toshio ^b   Caron, Kathleen M ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cardiac development; Epicardium; Hyperplasia; Mouse models; Myocardium

Indexed keywords

ADRENOMEDULLIN; CRE RECOMBINASE;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; DISEASE SEVERITY; EMBRYO DEVELOPMENT; EPICARDIUM; FIBROBLAST; GENE EXPRESSION; HEART DEVELOPMENT; HEART INFARCTION; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; WILD TYPE;

MUS;

ADRENOMEDULLIN; ANIMALS; BLOTTING, WESTERN; BROMODEOXYURIDINE; CELL CYCLE; DNA PRIMERS; GENETIC VECTORS; HEART; HYPERPLASIA; MICE; MICE, MUTANT STRAINS; MYOCARDIUM; MYOCYTES, CARDIAC; PERICARDIUM; REAL-TIME POLYMERASE CHAIN REACTION; RNA STABILITY; SIGNAL TRANSDUCTION;

EID: 84892671455     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24065     Document Type: Article

References (79)

1. Agah R, Frenkel PA, French BA, Michael LH, Overbeek PA, Schneider MD. 1997. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J Clin Invest 100:169-179.
2. Archbold JK, Flanagan JU, Watkins HA, Gingell JJ, Hay DL. 2011. Structural insights into RAMP modification of secretin family G protein-coupled receptors: implications for drug development. Trends Pharmacol Sci 32:591-600.
3. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, Washington MK, Neilson EG, Moses HL. 2004. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303:848-851.
4. Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, Stallcup WB, Denton CP, McCulloch A, Chen J, Evans SM. 2008. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454:104-108.
5. Caron K, Hagaman J, Nishikimi T, Kim HS, Smithies O. 2007. Adrenomedullin gene expression differences in mice do not affect blood pressure but modulate hypertension-induced pathology in males. Proc Natl Acad Sci U S A 104:3420-3425.
6. Caron KM, Smithies O. 2001. Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional Adrenomedullin gene. Proc Natl Acad Sci U S A 98:615-619.
7. Caron KM, Smithies O. 2002. Multiple roles of adrenomedullin revealed by animal models. Microsc Res Tech 57:55-59.
8. Chaudhry HW, Dashoush NH, Tang H, Zhang L, Wang X, Wu EX, Wolgemuth DJ. 2004. Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J Biol Chem 279:35858-35866.
9. Chen J, Kubalak SW, Chien KR. 1998. Ventricular muscle-restricted targeting of the RXRalpha gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development 125:1943-1949.
10. Chen T, Chang TC, Kang JO, Choudhary B, Makita T, Tran CM, Burch JB, Eid H, Sucov HM. 2002. Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev Biol 250:198-207.
11. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr. 1998. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 95:2979-2984.
12. Cornish J, Grey A, Callon KE, Naot D, Hill BL, Lin CQ, Balchin LM, Reid IR. 2004. Shared pathways of osteoblast mitogenesis induced by amylin, adrenomedullin, and IGF-1. Biochem Biophys Res Commun 318:240-246.
13. Dackor RT, Fritz-Six K, Dunworth WP, Gibbons CL, Smithies O, Caron KM. 2006. Hydrops fetalis, cardiovascular defects, and embryonic lethality in mice lacking the calcitonin receptor-like receptor gene. Mol Cell Biol 26:2511-2518.
14. Degenhardt K, Singh MK, Epstein JA. 2013. New approaches under development: cardiovascular embryology applied to heart disease. J Clin Invest 123:71-74.
15. Dhillon OS, Khan SQ, Narayan HK, Ng KH, Struck J, Quinn PA, Morgenthaler NG, Squire IB, Davies JE, Bergmann A, Ng LL. 2010. Prognostic value of mid-regional pro-adrenomedullin levels taken on admission and discharge in non-ST-elevation myocardial infarction: the LAMP (Leicester Acute Myocardial Infarction Peptide) II study. J Am Coll Cardiol 56:125-133.
16. Doods H, Arndt K, Rudolf K, Just S. 2007. CGRP antagonists: unravelling the role of CGRP in migraine. Trends Pharmacol Sci 28:580-587.
17. Duan J, Gherghe C, Liu D, Hamlett E, Srikantha L, Rodgers L, Regan JN, Rojas M, Willis M, Leask A, Majesky M, Deb A. 2012. Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J 31:429-442.
18. Fandrey J, Pagel H, Frede S, Wolff M, Jelkmann W. 1994. Thyroid hormones enhance hypoxia-induced erythropoietin production in vitro. Exp Hematol 22:272-277.
19. Franco-Montoya ML, Boucherat O, Thibault C, Chailley-Heu B, Incitti R, Delacourt C, Bourbon JR. 2011. Profiling target genes of FGF18 in the postnatal mouse lung: possible relevance for alveolar development. Physiol Genomics 43:1226-1240.
20. Fritz-Six KL, Dunworth WP, Li M, Caron KM. 2008. Adrenomedullin signaling is necessary for murine lymphatic vascular development. J Clin Invest 118:40-50.
21. Garayoa M, Martinez A, Lee S, Pio R, An WG, Neckers L, Trepel J, Montuenga LM, Ryan H, Johnson R, Gassmann M, Cuttitta F. 2000. Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis. Mol Endocrinol 14:848-862.
22. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G. 1995. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378:390-394.
23. Gittenberger-de Groot AC, Vrancken Peeters MP, Bergwerff M, Mentink MM, Poelmann RE. 2000. Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ Res 87:969-971.
24. Gittenberger-de Groot AC, Winter EM, Bartelings MM, Goumans MJ, DeRuiter MC, Poelmann RE. 2012. The arterial and cardiac epicardium in development, disease and repair. Differentiation 84:41-53.
25. Grego-Bessa J, Luna-Zurita L, del Monte G, Bolos V, Melgar P, Arandilla A, Garratt AN, Zang H, Mukouyama YS, Chen H, Shou W, Ballestar E, Esteller M, Rojas A, Perez-Pomares JM, de la Pompa JL. 2007. Notch signaling is essential for ventricular chamber development. Dev Cell 12:415-429.
26. Guadix JA, Ruiz-Villalba A, Lettice L, Velecela V, Munoz-Chapuli R, Hastie ND, Perez-Pomares JM, Martinez-Estrada OM. 2011. Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 138:1093-1097.
27. Guidolin D, Albertin G, Spinazzi R, Sorato E, Mascarin A, Cavallo D, Antonello M, Ribatti D. 2008. Adrenomedullin stimulates angiogenic response in cultured human vascular endothelial cells: Involvement of the vascular endothelial growth factor receptor 2. Peptides 29:2013-2023.
28. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, Martin JF. 2011. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332:458-461.
29. Huang GN, Thatcher JE, McAnally J, Kong Y, Qi X, Tan W, DiMaio JM, Amatruda JF, Gerard RD, Hill JA, Bassel-Duby R, Olson EN. 2012. C/EBP transcription factors mediate epicardial activation during heart development and injury. Science 338:1599-1603.
30. Ieda M, Tsuchihashi T, Ivey KN, Ross RS, Hong TT, Shaw RM, Srivastava D. 2009. Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 16:233-244.
31. Kakoki M, Tsai YS, Kim HS, Hatada S, Ciavatta DJ, Takahashi N, Arnold LW, Maeda N, Smithies O. 2004. Altering the expression in mice of genes by modifying their 3' regions. Dev Cell 6:597-606.
32. Karpinich NO, Hoopes SL, Kechele DO, Lenhart PM, Caron KM. 2011. Adrenomedullin function in vascular endothelial cells: insights from genetic mouse models. Curr Hypertens Rev 7:228-239.
33. Kataoka Y, Miyazaki S, Yasuda S, Nagaya N, Noguchi T, Yamada N, Morii I, Kawamura A, Doi K, Miyatake K, Tomoike H, Kangawa K. 2010. The first clinical pilot study of intravenous adrenomedullin administration in patients with acute myocardial infarction. J Cardiovasc Pharmacol 56:413-419.
34. Kerkela R, Kockeritz L, Macaulay K, Zhou J, Doble BW, Beahm C, Greytak S, Woulfe K, Trivedi CM, Woodgett JR, Epstein JA, Force T, Huggins GS. 2008. Deletion of GSK-3beta in mice leads to hypertrophic cardiomyopathy secondary to cardiomyoblast hyperproliferation. J Clin Invest 118:3609-3618.
35. Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G, Poss KD. 2011. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev Cell 20:397-404.
36. Kitamura K, Kangawa K, Kawamoto M, Ichiki Y, Nakamura S, Matsuo H, Eto T. 1993. Adrenomedullin: a novel hypotensive peptide isolated from human pheochromocytoma. Biochem Biophys Res Commun 192:553-560.
37. Krege JH, Hodgin JB, Hagaman JR, Smithies O. 1995. A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 25:1111-1115.
38. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. 1993. WT-1 is required for early kidney development. Cell 74:679-691.
39. Kubo A, Minamino N, Isumi Y, Katafuchi T, Kangawa K, Dohi K, Matsuo H. 1998. Production of adrenomedullin in macrophage cell line and peritoneal macrophage. J Biol Chem 273:16730-16738.
40. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA, Labow MA. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121:489-503.
41. Lavine KJ, Yu K, White AC, Zhang X, Smith C, Partanen J, Ornitz DM. 2005. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev Cell 8:85-95.
42. Lea R, Papalopulu N, Amaya E, Dorey K. 2009. Temporal and spatial expression of FGF ligands and receptors during Xenopus development. Dev Dyn 238:1467-1479.
43. Lee KF, Simon H, Chen H, Bates B, Hung MC, Hauser C. 1995. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378:394-398.
44. Li M, Schwerbrock NM, Lenhart PM, Fritz-Six KL, Kadmiel M, Christine KS, Kraus DM, Espenschied ST, Willcockson HH, Mack CP, Caron KM. 2013. Fetal-derived adrenomedullin mediates the innate immune milieu of the placenta. J Clin Invest 123:2408-2420.
45. Li P, Cavallero S, Gu Y, Chen TH, Hughes J, Hassan AB, Bruning JC, Pashmforoush M, Sucov HM. 2011. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138:1795-1805.
46. Lu SY, Sheikh F, Sheppard PC, Fresnoza A, Duckworth ML, Detillieux KA, Cattini PA. 2008. FGF-16 is required for embryonic heart development. Biochem Biophys Res Commun 373:270-274.
47. Maisel A, Mueller C, Nowak R, Peacock WF, Landsberg JW, Ponikowski P, Mockel M, Hogan C, Wu AH, Richards M, Clopton P, Filippatos GS, Di Somma S, Anand I, Ng L, Daniels LB, Neath SX, Christenson R, Potocki M, McCord J, Terracciano G, Kremastinos D, Hartmann O, von Haehling S, Bergmann A, Morgenthaler NG, Anker SD. 2010. Mid-region pro-hormone markers for diagnosis and prognosis in acute dyspnea: results from the BACH (Biomarkers in Acute Heart Failure) trial. J Am Coll Cardiol 55:2062-2076.
48. Maisel A, Mueller C, Nowak RM, Peacock WF, Ponikowski P, Mockel M, Hogan C, Wu AH, Richards M, Clopton P, Filippatos GS, Di Somma S, Anand I, Ng LL, Daniels LB, Neath SX, Christenson R, Potocki M, McCord J, Hartmann O, Morgenthaler NG, Anker SD. 2011. Midregion prohormone adrenomedullin and prognosis in patients presenting with acute dyspnea: results from the BACH (Biomarkers in Acute Heart Failure) trial. J Am Coll Cardiol 58:1057-1067.
49. Merki E, Zamora M, Raya A, Kawakami Y, Wang J, Zhang X, Burch J, Kubalak SW, Kaliman P, Izpisua Belmonte JC, Chien KR, Ruiz-Lozano P. 2005. Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc Natl Acad Sci U S A 102:18455-18460.
50. Meyer D, Birchmeier C. 1995. Multiple essential functions of neuregulin in development. Nature 378:386-390.
51. Minamino N, Shoji H, Sugo S, Kangawa K, Matsuo H. 1995. Adrenocortical steroids, thyroid hormones and retinoic acid augment the production of adrenomedullin in vascular smooth muscle cells. Biochem Biophys Res Commun 211:686-693.
52. Montuenga LM, Mariano JM, Prentice MA, Cuttitta F, Jakowlew SB. 1998. Coordinate expression of transforming growth factor-beta1 and adrenomedullin in rodent embryogenesis. Endocrinology 139:3946-3957.
53. Montuenga LM, Martinez A, Miller MJ, Unsworth EJ, Cuttitta F. 1997. Expression of adrenomedullin and its receptor during embryogenesis suggests autocrine or paracrine modes of action. Endocrinology 138:440-451.
54. Moses KA, DeMayo F, Braun RM, Reecy JL, Schwartz RJ. 2001. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31:176-180.
55. Nagaya N, Satoh T, Nishikimi T, Uematsu M, Furuichi S, Sakamaki F, Oya H, Kyotani S, Nakanishi N, Goto Y, Masuda Y, Miyatake K, Kangawa K. 2000. Hemodynamic, renal, and hormonal effects of adrenomedullin infusion in patients with congestive heart failure. Circulation 101:498-503.
56. Nishikimi T, Mori Y, Kobayashi N, Tadokoro K, Wang X, Akimoto K, Yoshihara F, Kangawa K, Matsuoka H. 2002. Renoprotective effect of chronic adrenomedullin infusion in Dahl salt-sensitive rats. Hypertension 39:1077-1082.
57. Nishikimi T, Tadokoro K, Mori Y, Wang X, Akimoto K, Yoshihara F, Minamino N, Kangawa K, Matsuoka H. 2003a. Ventricular adrenomedullin system in the transition from LVH to heart failure in rats. Hypertension 41:512-518.
58. Nishikimi T, Yoshihara F, Horinaka S, Kobayashi N, Mori Y, Tadokoro K, Akimoto K, Minamino N, Kangawa K, Matsuoka H. 2003b. Chronic administration of adrenomedullin attenuates transition from left ventricular hypertrophy to heart failure in rats. Hypertension 42:1034-1041.
59. Nishikimi T, Karasawa T, Inaba C, Ishimura K, Tadokoro K, Koshikawa S, Yoshihara F, Nagaya N, Sakio H, Kangawa K, Matsuoka H. 2009. Effects of long-term intravenous administration of adrenomedullin (AM) plus hANP therapy in acute decompensated heart failure: a pilot study. Circ J 73:892-898.
60. Pennisi DJ, Ballard VL, Mikawa T. 2003. Epicardium is required for the full rate of myocyte proliferation and levels of expression of myocyte mitogenic factors FGF2 and its receptor, FGFR-1, but not for transmural myocardial patterning in the embryonic chick heart. Dev Dyn 228:161-172.
61. Phillips MD, Mukhopadhyay M, Poscablo C, Westphal H. 2011. Dkk1 and Dkk2 regulate epicardial specification during mouse heart development. Int J Cardiol 150:186-192.
62. Qiu Z, Cang Y, Goff SP. 2010. c-Abl tyrosine kinase regulates cardiac growth and development. Proc Natl Acad Sci U S A 107:1136-1141.
63. Rademaker MT, Charles CJ, Lewis LK, Yandle TG, Cooper GJ, Coy DH, Richards AM, Nicholls MG. 1997. Beneficial hemodynamic and renal effects of adrenomedullin in an ovine model of heart failure. Circulation 96:1983-1990.
64. Rudat C, Kispert A. 2012. Wt1 and epicardial fate mapping. Circ Res 111:165-169.
65. Salvatore CA, Moore EL, Calamari A, Cook JJ, Michener MS, O'Malley S, Miller PJ, Sur C, Williams DL Jr, Zeng Z, Danziger A, Lynch JJ, Regan CP, Fay JF, Tang YS, Li CC, Pudvah NT, White RB, Bell IM, Gallicchio SN, Graham SL, Selnick HG, Vacca JP, Kane SA. 2010. Pharmacological properties of MK-3207, a potent and orally active calcitonin gene-related peptide receptor antagonist. J Pharmacol Exp Ther 333:152-160.
66. Schwenk F, Baron U, Rajewsky K. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23:5080-5081.
67. Shimosawa T, Shibagaki Y, Ishibashi K, Kitamura K, Kangawa K, Kato S, Ando K, Fujita T. 2002. Adrenomedullin, an endogenous peptide, counteracts cardiovascular damage. Circulation 105:106-111.
68. Shindo T, Kurihara Y, Nishimatsu H, Moriyama N, Kakoki M, Wang Y, Imai Y, Ebihara A, Kuwaki T, Ju KH, Minamino N, Kangawa K, Ishikawa T, Fukuda M, Akimoto Y, Kawakami H, Imai T, Morita H, Yazaki Y, Nagai R, Hirata Y, Kurihara H. 2001. Vascular abnormalities and elevated blood pressure in mice lacking adrenomedullin gene. Circulation 104:1964-1971.
69. Smart N, Bollini S, Dube KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu WT, Riley PR. 2011. De novo cardiomyocytes from within the activated adult heart after injury. Nature 474:640-644.
70. Stainier DY, Weinstein BM, Detrich HW III, Zon LI, Fishman MC. 1995. Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 121:3141-3150.
71. Stuckmann I, Evans S, Lassar AB. 2003. Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev Biol 255:334-349.
72. Sucov HM, Gu Y, Thomas S, Li P, Pashmforoush M. 2009. Epicardial control of myocardial proliferation and morphogenesis. Pediatr Cardiol 30:617-625.
73. Tomoda Y, Kikumoto K, Isumi Y, Katafuchi T, Tanaka A, Kangawa K, Dohi K, Minamino N. 2001. Cardiac fibroblasts are major production and target cells of adrenomedullin in the heart in vitro. Cardiovasc Res 49:721-730.
74. Trivedi CM, Lu MM, Wang Q, Epstein JA. 2008. Transgenic overexpression of Hdac3 in the heart produces increased postnatal cardiac myocyte proliferation but does not induce hypertrophy. J Biol Chem 283:26484-26489.
75. van Wijk B, Gunst QD, Moorman AF, van den Hoff MJ. 2012. Cardiac regeneration from activated epicardium. PLoS One 7:e44692.
76. Vega-Hernandez M, Kovacs A, De Langhe S, Ornitz DM. 2011. FGF10/FGFR2b signaling is essential for cardiac fibroblast development and growth of the myocardium. Development 138:3331-3340.
77. Viragh S, Gittenberger-de Groot AC, Poelmann RE, Kalman F. 1993. Early development of quail heart epicardium and associated vascular and glandular structures. Anat Embryol (Berl) 188:381-393.
78. Wu H, Lee SH, Gao J, Liu X, Iruela-Arispe ML. 1999. Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development 126:3597-3605.
79. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, Pu WT. 2008. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454:109-113.