Systemic, but not cardiomyocyte-specific, deletion of the natriuretic peptide receptor guanylyl cyclase A increases cardiomyocyte number in neonatal mice

Histochemistry and Cell Biology

Volumn 144, Issue 4, 2015, Pages 365-375

  Schipke, Julia ^a   Roloff, Konstanze ^c   Kuhn, Michaela ^c   Mühlfeld, Christian ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b German Center for Lung Research   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Atrial natriuretic peptide; Cardiomyocyte number; Guanylyl cyclase A; Hyperplasia; Hypertrophy

Indexed keywords

GUANYLATE CYCLASE; GUANYLYL CYCLASE A; UNCLASSIFIED DRUG; ATRIAL NATRIURETIC FACTOR RECEPTOR; NATRIURETIC PEPTIDE RECEPTOR A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COMPOSITION; CELL COUNT; CELL NUCLEUS; CELL PROLIFERATION; CELL VOLUME; CONTROLLED STUDY; ENZYME INACTIVATION; HEART DEVELOPMENT; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART WEIGHT; MOUSE; MUSCLE FIBRIL; NEWBORN; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SARCOPLASM; STEREOMETRY; ANIMAL; CARDIAC MUSCLE CELL; CARDIOMEGALY; COMPARATIVE STUDY; DEFICIENCY; ENZYMOLOGY; GENE DELETION; GENETICS; GENOTYPE; HYPERPLASIA; KNOCKOUT MOUSE; PATHOLOGY; PHENOTYPE;

ANIMALS; ANIMALS, NEWBORN; CARDIOMEGALY; CELL COUNT; CELL PROLIFERATION; GENE DELETION; GENOTYPE; HYPERPLASIA; MICE, KNOCKOUT; MYOCYTES, CARDIAC; PHENOTYPE; RECEPTORS, ATRIAL NATRIURETIC FACTOR;

EID: 84942367241     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-015-1337-z     Document Type: Article

References (53)

1. Anand-Srivastava MB, Trachte GJ (1993) Atrial natriuretic factor receptors and signal transduction mechanisms. Pharmacol Rev 45:455–497
2. Becker JR, Chatterjee S, Robinson TY, Bennett JS, Panakova D, Galindo CL, Zhong L, Shin JT, Coy SM, Kelly AE, Roden DM, Lim CC, MacRae CA (2014) Differential activation of natriuretic peptide receptors modulates cardiomyocyte proliferation during development. Development 141:335–345. doi:10.1242/dev.100370
3. Bruel A, Nyengaard JR (2005) Design-based stereological estimation of the total number of cardiac myocytes in histological sections. Basic Res Cardiol 100:311–319. doi:10.1007/s00395-005-0524-9
4. Cameron VA, Ellmers LJ (2003) Minireview: natriuretic peptides during development of the fetal heart and circulation. Endocrinology 144:2191–2194. doi:10.1210/en.2003-0127
5. Cameron VA, Aitken GD, Ellmers LJ, Kennedy MA, Espiner EA (1996) The sites of gene expression of atrial, brain, and C-type natriuretic peptides in mouse fetal development: temporal changes in embryos and placenta. Endocrinology 137:817–824. doi:10.1210/endo.137.3.8603590
6. Charng MJ, Frenkel PA, Lin Q, Yamada M, Schwartz RJ, Olson EN, Overbeek P, Schneider MD (1998) A constitutive mutation of ALK5 disrupts cardiac looping and morphogenesis in mice. Dev Biol 199:72–79
7. Cheung CY (1995) Regulation of atrial natriuretic factor secretion and expression in the ovine fetus. Neurosci Biobehav Rev 19:159–164
8. Cheung CY, Gibbs DM, Brace RA (1987) Atrial natriuretic factor in maternal and fetal sheep. Am J Physiol 252:E279–E282
9. de Bold AJ, Ma KK, Zhang Y, de Bold ML, Bensimon M, Khoshbaten A (2001) The physiological and pathophysiological modulation of the endocrine function of the heart. Can J Physiol Pharmacol 79:705–714
10. Deloof S, Chatelain A (1994) Effect of blood volume expansion on basal plasma atrial natriuretic factor and adrenocorticotropic hormone secretions in the fetal rat at term. Biol Neonate 65:390–395
11. Eisele JC, Schaefer IM, Randel NJ, Post H, Liebetanz D, Bruel A, Muhlfeld C (2008) Effect of voluntary exercise on number and volume of cardiomyocytes and their mitochondria in the mouse left ventricle. Basic Res Cardiol 103:12–21. doi:10.1007/s00395-007-0684-x
12. Fernandez E, Siddiquee Z, Shohet RV (2001) Apoptosis and proliferation in the neonatal murine heart. Dev Dyn 221:302–310. doi:10.1002/dvdy.1139
13. Garbers DL (1992) Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands. Cell 71:1–4
14. Gerdes AM, Moore JA, Hines JM, Kirkland PA, Bishop SP (1986) Regional differences in myocyte size in normal rat heart. Anat Rec 215:420–426. doi:10.1002/ar.1092150414
15. Giraud GD, Louey S, Jonker S, Schultz J, Thornburg KL (2006) Cortisol stimulates cell cycle activity in the cardiomyocyte of the sheep fetus. Endocrinology 147:3643–3649. doi:10.1210/en.2006-0061
16. Gruber C, Kohlstedt K, Loot AE, Fleming I, Kummer W, Muhlfeld C (2012a) Stereological characterization of left ventricular cardiomyocytes, capillaries, and innervation in the nondiabetic, obese mouse. Cardiovasc Pathol 21:346–354. doi:10.1016/j.carpath.2011.11.003
17. Gruber C, Nink N, Nikam S, Magdowski G, Kripp G, Voswinckel R, Muhlfeld C (2012b) Myocardial remodelling in left ventricular atrophy induced by caloric restriction. J Anat 220:179–185. doi:10.1111/j.1469-7580.2011.01453.x
18. Hersey RM, Nazir MA, Whitney KD, Klein RM, Sale RD, Hinton DA, Weisz J, Gattone VH (1989) Atrial natriuretic peptide in heart and specific binding in organs from fetal and newborn rats. Cell Biochem Funct 7:35–41. doi:10.1002/cbf.290070107
19. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, Zetsche B, Hammer RE, Herz J, Kuhn M (2002) Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci USA 99:7142–7147. doi:10.1073/pnas.102650499
20. Holtwick R, van EM, Skryabin BV, Baba HA, Bubikat A, Begrow F, Schneider MD, Garbers DL, Kuhn M (2003) Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J Clin Invest 111:1399–1407. doi:10.1172/JCI17061
21. James TN (1998) Normal and abnormal consequences of apoptosis in the human heart. Annu Rev Physiol 60:309–325. doi:10.1146/annurev.physiol.60.1.309
22. Kishimoto I, Rossi K, Garbers DL (2001) A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc Natl Acad Sci USA 98:2703–2706. doi:10.1073/pnas.051625598
23. Klaiber M, Kruse M, Volker K, Schroter J, Feil R, Freichel M, Gerling A, Feil S, Dietrich A, Londono JE, Baba HA, Abramowitz J, Birnbaumer L, Penninger JM, Pongs O, Kuhn M (2010) Novel insights into the mechanisms mediating the local antihypertrophic effects of cardiac atrial natriuretic peptide: role of cGMP-dependent protein kinase and RGS2. Basic Res Cardiol 105:583–595. doi:10.1007/s00395-010-0098-z
24. Knowles JW, Esposito G, Mao L, Hagaman JR, Fox JE, Smithies O, Rockman HA, Maeda N (2001) Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest 107:975–984. doi:10.1172/JCI11273
25. Kuhn M (2003) Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ Res 93:700–709. doi:10.1161/01.RES.0000094745.28948.4D
26. Kuhn M (2004) Molecular physiology of natriuretic peptide signalling. Basic Res Cardiol 99:76–82. doi:10.1007/s00395-004-0460-0
27. Kuhn M, Holtwick R, Baba HA, Perriard JC, Schmitz W, Ehler E (2002) Progressive cardiac hypertrophy and dysfunction in atrial natriuretic peptide receptor (GC-A) deficient mice. Heart 87:368–374
28. Lopez MJ, Wong SK, Kishimoto I, Dubois S, Mach V, Friesen J, Garbers DL, Beuve A (1995) Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature 378:65–68. doi:10.1038/378065a0
29. Matsukawa N, Grzesik WJ, Takahashi N, Pandey KN, Pang S, Yamauchi M, Smithies O (1999) The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc Natl Acad Sci USA 96:7403–7408
30. Mattfeldt T, Mall G, Gharehbaghi H, Moller P (1990) Estimation of surface area and length with the orientator. J Microsc 159:301–317
31. Mendez J, Keys A (1961) Density and composition of mammalian muscle. Metabolism 9:184–188
32. Morkin E (1993) Regulation of myosin heavy chain genes in the heart. Circulation 87:1451–1460
33. Muhlfeld C, Ochs M (2014) Measuring structure—What’s the point in counting? Ann Anat 196:1–2. doi:10.1016/j.aanat.2013.09.002
34. Muhlfeld C, Singer D, Engelhardt N, Richter J, Schmiedl A (2005) Electron microscopy and microcalorimetry of the postnatal rat heart (Rattus norvegicus). Comp Biochem Physiol A Mol Integr Physiol 141:310–318. doi:10.1016/j.cbpb.2005.06.001
35. Muhlfeld C, Nyengaard JR, Mayhew TM (2010) A review of state-of-the-art stereology for better quantitative 3D morphology in cardiac research. Cardiovasc Pathol 19:65–82. doi:10.1016/j.carpath.2008.10.015
36. Nyengaard JR, Gundersen HJ (1992) The isector: a simple and direct method for generating isotropic, uniform random sections from small specimens. J Microsc 165:427–431. doi:10.1111/j.1365-2818.1992.tb01497.x
37. Oliver PM, Fox JE, Kim R, Rockman HA, Kim HS, Reddick RL, Pandey KN, Milgram SL, Smithies O, Maeda N (1997) Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc Natl Acad Sci USA 94:14730–14735
38. O’Tierney PF, Chattergoon NN, Louey S, Giraud GD, Thornburg KL (2010) Atrial natriuretic peptide inhibits angiotensin II-stimulated proliferation in fetal cardiomyocytes. J Physiol 588:2879–2889. doi:10.1113/jphysiol.2010.191098
39. Pandey KN (2008) Emerging roles of natriuretic peptides and their receptors in pathophysiology of hypertension and cardiovascular regulation. J Am Soc Hypertens 2:210–226. doi:10.1016/j.jash.2008.02.001
40. Pandey KN (2011) Guanylyl cyclase/atrial natriuretic peptide receptor-A: role in the pathophysiology of cardiovascular regulation. Can J Physiol Pharmacol 89:557–573. doi:10.1139/y11-054
41. Pandey KN, Singh S (1990) Molecular cloning and expression of murine guanylate cyclase/atrial natriuretic factor receptor cDNA. J Biol Chem 265:12342–12348
42. Rosenfeld CR, Samson WK, Roy TA, Faucher DJ, Magness RR (1992) Vasoconstrictor-induced secretion of ANP in fetal sheep. Am J Physiol 263:E526–E533
43. Rosenzweig A, Seidman CE (1991) Atrial natriuretic factor and related peptide hormones. Annu Rev Biochem 60:229–255. doi:10.1146/annurev.bi.60.070191.001305
44. Rubattu S, Sciarretta S, Morriello A, Calvieri C, Battistoni A, Volpe M (2010) NPR-C: a component of the natriuretic peptide family with implications in human diseases. J Mol Med (Berl) 88:889–897. doi:10.1007/s00109-010-0641-2
45. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93:13176–13181
46. Shi SJ, Nguyen HT, Sharma GD, Navar LG, Pandey KN (2001) Genetic disruption of atrial natriuretic peptide receptor-A alters renin and angiotensin II levels. Am J Physiol Renal Physiol 281:F665–F673
47. Skryabin BV, Holtwick R, Fabritz L, Kruse MN, Veltrup I, Stypmann J, Kirchhof P, Sabrane K, Bubikat A, Voss M, Kuhn M (2004) Hypervolemic hypertension in mice with systemic inactivation of the (floxed) guanylyl cyclase-A gene by alphaMHC-Cre-mediated recombination. Genesis 39:288–298. doi:10.1002/gene.20056
48. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136
49. Sundgren NC, Giraud GD, Stork PJ, Maylie JG, Thornburg KL (2003) Angiotensin II stimulates hyperplasia but not hypertrophy in immature ovine cardiomyocytes. J Physiol 548:881–891. doi:10.1113/jphysiol.2003.038778
50. Takahashi T, Allen PD, Izumo S (1992) Expression of A-, B-, and C-type natriuretic peptide genes in failing and developing human ventricles. Correlation with expression of the Ca(2+)-ATPase gene. Circ Res 71:9–17
51. Thornburg K, Jonker S, O’Tierney P, Chattergoon N, Louey S, Faber J, Giraud G (2011) Regulation of the cardiomyocyte population in the developing heart. Prog Biophys Mol Biol 106:289–299. doi:10.1016/j.pbiomolbio.2010.11.010
52. Weibel ER (1979) Stereological methods. Vol I: Practical methods for biological morphometry. Academic Press, London
53. Wu CF, Bishopric NH, Pratt RE (1997) Atrial natriuretic peptide induces apoptosis in neonatal rat cardiac myocytes. J Biol Chem 272:14860–14866