Activation of IGF-2R stimulates cardiomyocyte hypertrophy in the late gestation sheep fetus

Journal of Physiology

Volumn 590, Issue 21, 2012, Pages 5425-5437

  Wang, Kimberley C W ^a   Brooks, Doug A ^a   Thornburg, Kent L ^b   Morrison, Janna L ^a  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA Q; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LEUCINE; LEUCINE 2 SOMATOMEDIN B RECEPTOR; RECOMBINANT SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD GAS; BLOOD PRESSURE; CELL ISOLATION; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; CORONARY ARTERY CIRCUMFLEX BRANCH; ENZYME ACTIVATION; EWE; FETUS; FETUS WEIGHT; GESTATIONAL AGE; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; CORONARY VESSELS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FETUS; GESTATIONAL AGE; HEART VENTRICLES; HYPERTROPHY; INSULIN-LIKE GROWTH FACTOR II; MYOCYTES, CARDIAC; RECEPTOR, IGF TYPE 2; SHEEP;

EID: 84868103395     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.238410     Document Type: Article

References (51)

1. Barbera A, Giraud GD, Reller MD, Maylie J, Morton MJ & Thornburg KL (2000). Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 279, R1157-R1164.
2. Barker DJ (1995). Fetal origins of coronary heart disease. BMJ 311, 171-174.
3. Barki-Harrington L, Perrino C & Rockman HA (2004). Network integration of the adrenergic system in cardiac hypertrophy. Cardiovasc Res 63, 391-402.
4. Bauman RP, Rembert JC, Himmelstein SI, Klotman PE & Greenfield JC Jr (1987). Effect of atrial natriuretic factor on transmural myocardial blood flow distribution in the dog. Circulation 76, 705-709.
5. Bensley JG, Stacy VK, De Matteo R, Harding R & Black MJ (2010). Cardiac remodelling as a result of pre-term birth: implications for future cardiovascular disease. Eur Heart J 31, 2058-2066.
6. Böhm M, Moll M, Schmid B, Paul M, Ganten D, Castellano M & Erdmann E (1994). β-Adrenergic neuroeffector mechanisms in cardiac hypertrophy of renin transgenic rats. Hypertension 24, 653-662.
7. Bokník P, Heinroth-Hoffmanb I, Kirchhefer U, Knapp J, Linck B, Lüss H, Müller T, Schmitz W, Brodde OE & Neumann J (2001). Enhanced protein phosphorylation in hypertensive hypertrophy. Cardiovasc Res 51, 717-728.
8. Botting KJ, Wang KC, Padhee M, McMillen IC, Summers-Pearce B, Rattanatray L, Cutri N, Posterino GS, Brooks DA & Morrison JL (2011). Early origins of heart disease: low birth weight and determinants of cardiomyocyte endowment. Clin Exp Pharmacol Physiol 39, 814-823.
9. Brüel A, Oxlund H & Nyengaard JR (2005). The total length of myocytes and capillaries, and total number of myocyte nuclei in the rat heart are time-dependently increased by growth hormone. Growth Horm IGF Res 15, 256-264.
10. Buxton IL & Brunton LL (1983). Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J Biol Chem 258, 10233-10239.
11. Chen RJ, Wu HC, Chang MH, Lai CH, Tien YC, Hwang JM, Kuo WH, Tsai FJ, Tsai CH, Chen LM, Huang CY & Chu CH (2009). Leu27IGF2 plays an opposite role to IGF1 to induce H9c2 cardiomyoblast cell apoptosis via Gaq signaling. J Mol Endocrinol 43, 221-230.
12. Chijiwa T, Mishima A, Hagiwara M, Sano M, Hayashi K, Inoue T, Naito K, Toshioka T & Hidaka H (1990). Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J Biol Chem 265, 5267-5272.
13. Chu CH, Huang CY, Lu MC, Lin JA, Tsai FJ, Tsai CH, Chu CY, Kuo WH, Chen LM & Chen LY (2009a). Enhancement of AG1024-induced H9c2 cardiomyoblast cell apoptosis via the interaction of IGF2R with Gα proteins and its downstream PKA and PLC-β modulators by IGF-II. Chin J Physiol 52, 31-37.
14. Chu CH, Tzang BS, Chen LM, Kuo CH, Cheng YC, Chen LY, Tsai FJ, Tsai CH, Kuo WW & Huang CY (2008). IGF-II/mannose-6-phosphate receptor signaling induced cell hypertrophy and atrial natriuretic peptide/BNP expression via Gαq interaction and protein kinase C-α/CaMKII activation in H9c2 cardiomyoblast cells. J Endocrinol 197, 381-390.
15. Chu CH, Tzang BS, Chen LM, Liu CJ, Tsai FJ, Tsai CH, Lin JA, Kuo WW, Bau DT, Yao CH & Huang CY (2009b). Activation of insulin-like growth factor II receptor induces mitochondrial-dependent apoptosis through Gaq and downstream calcineurin signaling in myocardial cells. Endocrinology 150, 2723-2731.
16. D'Angelo DD, Sakata Y, Lorenz JN, Boivin GP, Walsh RA, Liggett SB & Dorn GW II (1997). Transgenic Gαq overexpression induces cardiac contractile failure in mice. Proc Natl Acad Sci U S A 94, 8121-8126.
17. Danielson L, McMillen IC, Dyer JL & Morrison JL (2005). Restriction of placental growth results in greater hypotensive response to a-adrenergic blockade in fetal sheep during late gestation. J Physiol 563, 611-620.
18. Drummond G (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
19. Edwards LJ, Simonetta G, Owens JA, Robinson JS & McMillen IC (1999). Restriction of placental and fetal growth in sheep alters fetal blood pressure responses to angiotensin II and captopril. J Physiol 515, 897-904.
20. Giraud GD, Louey S, Jonker SS, Schultz J & Thornburg KL (2006). Cortisol stimulates cell cycle activity in the cardiomyocyte of the sheep fetus. Endocrinology 147, 3643-3649.
21. Gonzalez GA, Yamamoto KK, Fischer WH, Karr D, Menzel P, Biggs W 3rd, Vale WW & Montminy MR (1989). A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 337, 749-752.
22. Hawkins P, Steyn C, Ozaki T, Saito T, Noakes DE & Hanson MA (2000). Effect of maternal undernutrition in early gestation on ovine fetal blood pressure and cardiovascular reflexes. Am J Physiol Regul Integr Comp Physiol 279, R340-R348.
23. Huang CY, Hao LY & Buetow DE (2002). Hypertrophy of cultured adult rat ventricular cardiomyocytes induced by antibodies against the insulin-like growth factor (IGF)-I or the IGF-I receptor is IGF-II-dependent. Mol Cell Biochem 233, 65-72.
24. Jonker SS, Faber JJ, Anderson DF, Thornburg KL, Louey S & Giraud GD (2007a). Sequential growth of fetal sheep cardiac myocytes in response to simultaneous arterial and venous hypertension. Am J Physiol Regul Integr Comp Physiol 292, R913-R919.
25. Jonker SS, Zhang L, Louey S, Giraud GD, Thornburg KL & Faber JJ (2007b). Myocyte enlargement, differentiation, and proliferation kinetics in the fetal sheep heart. J Appl Physiol 102, 1130-1142.
26. Kannel WB, Levy D & Cupples LA (1987). Left ventricular hypertrophy and risk of cardiac failure: insights from the Framingham Study. J Cardiovasc Pharmacol 10, S135-140.
27. Kornfeld S (1992). Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem 61, 307-330.
28. Lavandero S, Foncea R, Pérez V & Sapag-Hagar M (1998). Effect of inhibitors of signal transduction on IGF-1-induced protein synthesis associated with hypertrophy in cultured neonatal rat ventricular myocytes. FEBS Lett 422, 193-196.
29. Levy D, Garrison RJ, Savage DD, Kannel WB & Castelli WP (1990). Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med 322, 1561-1566.
30. McConnell BK, Moravec CS & Bond M (1998). Troponin I phosphorylation and myofilament calcium sensitivity during decompensated cardiac hypertrophy. Am J Physiol Heart Circ Physiol 274, H385-H396.
31. Morrison JL, Botting KJ, Dyer JL, Williams SJ, Thornburg KL & McMillen IC (2007). Restriction of placental function alters heart development in the sheep fetus. Am J Physiol Regul Integr Comp Physiol 293, R306-R313.
32. Morrison JL, Carmichael L, Homan J & Richardson BS (1997). The effects of 'sleep promoting agents' on behavioural state in the ovine fetus. Brain Res Dev Brain Res 103, 1-8.
33. Morrison JL, Chien C, Gruber N, Rurak D & Riggs W (2001). Fetal behavioural state changes following maternal fluoxetine infusion in sheep. Brain Res Dev Brain Res 131, 47-56.
34. Muhlhausler BS, Duffield JA, Ozanne SE, Pilgrim C, Turner N, Morrison JL & McMillen IC (2009). The transition from fetal growth restriction to accelerated postnatal growth: a potential role for insulin signalling in skeletal muscle. J Physiol 587, 4199-4211.
35. Nishimoto I (1993). The IGF-II receptor system: a G protein-linked mechanism. Mol Reprod Dev 35, 398-406.
36. 2+-stimulated MgATPase of reconstituted actomyosin S-1. J Biol Chem 270, 25445-25454.
37. Oakley C (1971). Ventricular hypertrophy in cardiomyopathy. Br Heart J 33, 179-186.
38. Oh Y, Müller HL, Zhang H, Ling N & Rosenfeld RG (1993). Synthesis and characterization of IGF-II analogs: Applications in the evaluation of IGF receptor function and IGF-independent actions of IGFBPs. Adv Exp Med Biol 343, 41-54.
39. Posterino GS, Dunn SL, Botting KJ, Wang W, Gentili S & Morrison JL (2011). Changes in cardiac troponins with gestational age explain changes in cardiac muscle contractility in the sheep fetus. J Appl Physiol 111, 236-243.
40. Powell K, Rooke JA, McEvoy TG, Ashworth CJ, Robinson JJ, Wilmut I, Young LE & Sinclair KD (2006). Zygote donor nitrogen metabolism and in vitro embryo culture perturbs in utero development and IGF2R expression in ovine fetal tissues. Theriogenology 66, 1901-1912.
41. Reini SA, Wood CE & Keller-Wood M (2009). The ontogeny of genes related to ovine fetal cardiac growth. Gene Expr Patterns 9, 122-128.
42. Rich-Edwards J, Stampfer MJ, Manson JE, Rosner B, Hankinson SE, Colditz GA, Willett WC & Hennekens CH (1997). Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 315, 396-400.
43. Rudolph AM, Roman C & Gournay V (1999). Perinatal myocardial DNA and protein changes in the lamb: effect of cortisol in the fetus. Pediatr Res 46, 141-146.
44. Sakano K, Enjoh T, Numata F, Fujiwarat H, Marumoto Y, Higashihashi N, Sato Y, Perduell JF & Fujita-Yamaguchi Y (1991). The design, expression, and characterization of human insulin-like growth factor II (IGF-II) mutants specific for either the IGF-II/cation-independent mannose 6-phosphate receptor or IGF-I receptor. J Biol Chem 266, 20626-20635.
45. Skalhegg BS & Tasken K (2000). Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA. Front Biosci 5, D678-693.
46. Sundgren NC, Giraud GD, Schultz JM, Lasarev MR, Stork PJ & Thornburg KL (2003). Extracellular signal-regulated kinase and phosphoinositol-3 kinase mediate IGF-1 induced proliferation of fetal sheep cardiomyocytes. Am J Physiol Regul Integr Comp Physiol 285, R1481-R1489.
47. Wang KC, Brooks DA, Botting KJ & Morrison JL (2012). IGF-2R-mediated signaling results in hypertrophy of cultured cardiomyocytes from fetal sheep. Biol Reprod 86, 183.
48. Wang KC, Zhang L, McMillen IC, Botting KJ, Duffield JA, Zhang S, Suter CM, Brooks DA & Morrison JL (2011). Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb. J Physiol 589, 4709-4722.
49. Woodcock EA & Matkovich SJ (2005). Cardiomyocytes structure, function and associated pathologies. Int J Biochem Cell Biol 37, 1746-1751.
50. Yue TL, Gu JL, Wang C, Reith AD, Lee JC, Mirabilei RC, Kreutz R, Wang Y, Maleeffi B, Parsons AA & Ohlstein EH (2000). Extracellular signal-regulated kinase plays an essential role in hypertrophic agonists, endothelin-1 and phenylephrine-induced cardiomyocyte hypertrophy. J Biol Chem 275, 37895-37901.
51. Zou Y, Komuro I, Yamazaki T, Kudoh S, Uozumi H, Kadowaki T & Yazaki Y (1999). Both Gs and Gi proteins are critically involved in isoproterenol-induced cardiomyocyte hypertrophy. J Biol Chem 274, 9760-9770.