C-type natriuretic peptide facilitates autonomic Ca²⁺ entry in growth plate chondrocytes for stimulating bone growth

Ahrens MJ, Dudley AT. 2011. Chemical pretreatment of growth plate cartilage increases immunofluorescence

sensitivity. The Journal of Histochemistry and Cytochemistry 59:408–418. DOI: https://doi.org/10.1369/​

0022155411400869, PMID: 21411811

Miyazaki, Ichimura, et al. eLife 2022;11:e71931. DOI: https://doi.org/10.7554/eLife.71931

21 of 23

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

Cell Biology

Research article

Berendsen AD, Olsen BR. 2015. Bone development. Bone 80:14–18. DOI: https://doi.org/10.1016/j.bone.2015.​

04.035, PMID: 26453494

Bibli S-­I, Andreadou I, Chatzianastasiou A, Tzimas C, Sanoudou D, Kranias E, Brouckaert P, Coletta C, Szabo C,

Kremastinos DT, Iliodromitis EK, Papapetropoulos A. 2015. Cardioprotection by H2S engages a cGMP-­

dependent protein kinase G/phospholamban pathway. Cardiovascular Research 106:432–442. DOI: https://doi.​

org/10.1093/cvr/cvv129, PMID: 25870184

Clark RB, Hatano N, Kondo C, Belke DD, Brown BS, Kumar S, Votta BJ, Giles WR. 2010. Voltage-­gated K+

currents in mouse articular chondrocytes regulate membrane potential. Channels (Austin, Tex.) 4:179–191. DOI:

https://doi.org/10.4161/chan.4.3.11629, PMID: 20372061

Dong D-­L, Yue P, Yang B-­F, Wang W-­H. 2008. Hydrogen peroxide stimulates the Ca(2+)-­activated big-­

conductance K channels (BK) through cGMP signaling pathway in cultured human endothelial cells. Cellular

Physiology and Biochemistry 22:119–126. DOI: https://doi.org/10.1159/000149789, PMID: 18769038

Fleig A, Chubanov V. 2014. TRPM7. Fleig A (Ed). Handbook of Experimental Pharmacology. Springer. p.

521–546. DOI: https://doi.org/10.1007/978-3-642-54215-2_21, PMID: 24756720

Fukao M, Mason HS, Britton FC, Kenyon JL, Horowitz B, Keef KD. 1999. Cyclic GMP-­dependent protein kinase

activates cloned BKCa channels expressed in mammalian cells by direct phosphorylation at serine 1072. The

Journal of Biological Chemistry 274:10927–10935. DOI: https://doi.org/10.1074/jbc.274.16.10927, PMID:

10196172

Guo JY, Zhang MH, Jiang JZ, Piao LH, Fang XS, Jin Z, Cai YL. 2018. The role of CNP-­mediated PKG/PKA-­PLCβ

pathway in diabetes-­induced gastric motility disorder. Peptides 110:47–55. DOI: https://doi.org/10.1016/j.​

peptides.2018.10.012, PMID: 30391424

Houston DA, Staines KA, MacRae VE, Farquharson C. 2016. Culture of Murine Embryonic Metatarsals: A

Physiological Model of Endochondral Ossification. Journal of Visualized Experiments 1:e54978. DOI: https://​

doi.org/10.3791/54978, PMID: 28060328

Huang J, Zhou H, Mahavadi S, Sriwai W, Murthy KS. 2007. Inhibition of Galphaq-­dependent PLC-­beta1 activity

by PKG and PKA is mediated by phosphorylation of RGS4 and GRK2. American Journal of Physiology. Cell

Physiology 292:C200–C208. DOI: https://doi.org/10.1152/ajpcell.00103.2006, PMID: 16885398

Iwai T, Murai J, Yoshikawa H, Tsumaki N. 2008. Smad7 Inhibits chondrocyte differentiation at multiple steps

during endochondral bone formation and down-­regulates p38 MAPK pathways. The Journal of Biological

Chemistry 283:27154–27164. DOI: https://doi.org/10.1074/jbc.M801175200, PMID: 18644788

Kawasaki Y, Kugimiya F, Chikuda H, Kamekura S, Ikeda T, Kawamura N, Saito T, Shinoda Y, Higashikawa A,

Yano F, Ogasawara T, Ogata N, Hoshi K, Hofmann F, Woodgett JR, Nakamura K, Chung U, Kawaguchi H. 2008.

Phosphorylation of GSK-­3beta by cGMP-­dependent protein kinase II promotes hypertrophic differentiation of

murine chondrocytes. The Journal of Clinical Investigation 118:2506–2515. DOI: https://doi.org/10.1172/​

JCI35243, PMID: 18551195

Krejci P, Masri B, Fontaine V, Mekikian PB, Weis M, Prats H, Wilcox WR. 2005. Interaction of fibroblast growth

factor and C-­natriuretic peptide signaling in regulation of chondrocyte proliferation and extracellular matrix

homeostasis. Journal of Cell Science 118:5089–5100. DOI: https://doi.org/10.1242/jcs.02618, PMID: 16234329

Kubacka M, Kotańska M, Kazek G, Waszkielewicz AM, Marona H, Filipek B, Mogilski S. 2018. Involvement of the

NO/sGC/cGMP/K+ channels pathway in vascular relaxation evoked by two non-­quinazoline α1-­adrenoceptor

antagonists. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie 103:157–166. DOI: https://​

doi.org/10.1016/j.biopha.2018.04.034, PMID: 29653360

Lalli MJ, Shimizu S, Sutliff RL, Kranias EG, Paul RJ. 1999. [Ca2+]i homeostasis and cyclic nucleotide relaxation in

aorta of phospholamban-­deficient mice. The American Journal of Physiology 277:H963–H970. DOI: https://doi.​

org/10.1152/ajpheart.1999.277.3.H963, PMID: 10484417

Li Y, Ahrens MJ, Wu A, Liu J, Dudley AT. 2011. Calcium/calmodulin-­dependent protein kinase II activity regulates

the proliferative potential of growth plate chondrocytes. Development (Cambridge, England) 138:359–370.

DOI: https://doi.org/10.1242/dev.052324, PMID: 21177348

Liang L, Li X, Moutton S, Schrier Vergano SA, Cogné B, Saint-­Martin A, Hurst ACE, Hu Y, Bodamer O,

Thevenon J, Hung CY, Isidor B, Gerard B, Rega A, Nambot S, Lehalle D, Duffourd Y, Thauvin-­Robinet C,

Faivre L, Bézieau S, et al. 2019. De novo loss-­of-­function KCNMA1 variants are associated with a new multiple

malformation syndrome and a broad spectrum of developmental and neurological phenotypes. Human

Molecular Genetics 28:2937–2951. DOI: https://doi.org/10.1093/hmg/ddz117, PMID: 31152168

Liu F, Xu L, Nishi M, Ichimura A, Takeshima H. 2021. Enhanced Ca2+ handling in thioglycolate-­elicited peritoneal

macrophages. Cell Calcium 96:102381. DOI: https://doi.org/10.1016/j.ceca.2021.102381, PMID: 33647639

Martel G, Hamet P, Tremblay J. 2010. Central role of guanylyl cyclase in natriuretic peptide signaling in

hypertension and metabolic syndrome. Molecular and Cellular Biochemistry 334:53–65. DOI: https://doi.org/​

10.1007/s11010-009-0326-8, PMID: 19937369

Miyazawa T, Ogawa Y, Chusho H, Yasoda A, Tamura N, Komatsu Y, Pfeifer A, Hofmann F, Nakao K. 2002. Cyclic

GMP-­dependent protein kinase II plays a critical role in C-­type natriuretic peptide-­mediated endochondral

ossification. Endocrinology 143:3604–3610. DOI: https://doi.org/10.1210/en.2002-220307, PMID: 12193576

Mouser VHM, Melchels FPW, Visser J, Dhert WJA, Gawlitta D, Malda J. 2016. Yield stress determines

bioprintability of hydrogels based on gelatin-­methacryloyl and gellan gum for cartilage bioprinting.

Biofabrication 8:035003. DOI: https://doi.org/10.1088/1758-5090/8/3/035003, PMID: 27431733

Nakao K, Itoh H, Saito Y, Mukoyama M, Ogawa Y. 1996. The natriuretic peptide family Curr Opin Nephrol

Hypertens. Current Opinion in Nephrology and Hypertension 5:4–11. DOI: https://doi.org/10.1097/00041552-​

199601000-00003

Miyazaki, Ichimura, et al. eLife 2022;11:e71931. DOI: https://doi.org/10.7554/eLife.71931

22 of 23

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

Cell Biology

Research article

Nakao K, Osawa K, Yasoda A, Yamanaka S, Fujii T, Kondo E, Koyama N, Kanamoto N, Miura M, Kuwahara K,

Akiyama H, Bessho K, Nakao K. 2015. The Local CNP/GC-­B system in growth plate is responsible for

physiological endochondral bone growth. Scientific Reports 5:10554. DOI: https://doi.org/10.1038/srep10554,

PMID: 26014585

Nalli AD, Kumar DP, Al-­Shboul O, Mahavadi S, Kuemmerle JF, Grider JR, Murthy KS. 2014. Regulation of

Gβγi-­dependent PLC-β3 activity in smooth muscle: inhibitory phosphorylation of PLC-β3 by PKA and PKG and

stimulatory phosphorylation of Gαi-­GTPase-­activating protein RGS2 by PKG. Cell Biochemistry and Biophysics

70:867–880. DOI: https://doi.org/10.1007/s12013-014-9992-6, PMID: 24777815

Peake NJ, Hobbs AJ, Pingguan-­Murphy B, Salter DM, Berenbaum F, Chowdhury TT. 2014. Role of C-­type

natriuretic peptide signalling in maintaining cartilage and bone function. Osteoarthritis and Cartilage 22:1800–

1807. DOI: https://doi.org/10.1016/j.joca.2014.07.018, PMID: 25086404

Qian N, Ichimura A, Takei D, Sakaguchi R, Kitani A, Nagaoka R, Tomizawa M, Miyazaki Y, Miyachi H, Numata T,

Kakizawa S, Nishi M, Mori Y, Takeshima H. 2019. TRPM7 channels mediate spontaneous Ca2+ fluctuations in

growth plate chondrocytes that promote bone development. Science Signaling 12:eaaw4847. DOI: https://doi.​

org/10.1126/scisignal.aaw4847, PMID: 30967513

Raeymaekers L, Hofmann F, Casteels R. 1988. Cyclic GMP-­dependent protein kinase phosphorylates

phospholamban in isolated sarcoplasmic reticulum from cardiac and smooth muscle. The Biochemical Journal

252:269–273. DOI: https://doi.org/10.1042/bj2520269, PMID: 2844148

Savarirayan R, Tofts L, Irving M, Wilcox W, Bacino CA, Hoover-­Fong J, Ullot Font R, Harmatz P, Rutsch F,

Bober MB, Polgreen LE, Ginebreda I, Mohnike K, Charrow J, Hoernschemeyer D, Ozono K, Alanay Y, Arundel P,

Kagami S, Yasui N, et al. 2020. Once-­daily, subcutaneous vosoritide therapy in children with achondroplasia: a

randomised, double-­blind, phase 3, placebo-­controlled, multicentre trial. Lancet (London, England) 396:684–

692. DOI: https://doi.org/10.1016/S0140-6736(20)31541-5, PMID: 32891212

Ueda Y, Yasoda A, Yamashita Y, Kanai Y, Hirota K, Yamauchi I, Kondo E, Sakane Y, Yamanaka S, Nakao K, Fujii T,

Inagaki N. 2016. C-­type natriuretic peptide restores impaired skeletal growth in a murine model of

glucocorticoid-­induced growth retardation. Bone 92:157–167. DOI: https://doi.org/10.1016/j.bone.2016.08.​

026, PMID: 27594049

Vasques GA, Arnhold IJP, Jorge AAL. 2014. Role of the natriuretic peptide system in normal growth and growth

disorders. Hormone Research in Paediatrics 82:222–229. DOI: https://doi.org/10.1159/000365049, PMID:

25196103

White RE, Kryman JP, El-­Mowafy AM, Han G, Carrier GO. 2000. cAMP-­dependent vasodilators cross-­activate the

cGMP-­dependent protein kinase to stimulate BK(Ca) channel activity in coronary artery smooth muscle cells.

Circulation Research 86:897–905. DOI: https://doi.org/10.1161/01.res.86.8.897, PMID: 10785513

Wit JM, Camacho-­Hübner C. 2011. Endocrine regulation of longitudinal bone growth. Endocrine Development

21:30–41. DOI: https://doi.org/10.1159/000328119, PMID: 21865752

Wit JM, Oostdijk W, Losekoot M, van Duyvenvoorde HA, Ruivenkamp CAL, Kant SG. 2016. MECHANISMS IN

ENDOCRINOLOGY: Novel genetic causes of short stature. European Journal of Endocrinology 174:R145–

R173. DOI: https://doi.org/10.1530/EJE-15-0937, PMID: 26578640

Xia C, Bao Z, Yue C, Sanborn BM, Liu M. 2001. Phosphorylation and regulation of G-­protein-­activated

phospholipase C-­beta 3 by cGMP-­dependent protein kinases. The Journal of Biological Chemistry 276:19770–

19777. DOI: https://doi.org/10.1074/jbc.M006266200, PMID: 11278298

Yamashita T, Fujii T, Yamauchi I, Ueda Y, Hirota K, Kanai Y, Yasoda A, Inagaki N. 2020. C-­Type Natriuretic Peptide

Restores Growth Impairment Under Enzyme Replacement in Mice With Mucopolysaccharidosis VII.

Endocrinology 161:bqaa008. DOI: https://doi.org/10.1210/endocr/bqaa008, PMID: 31974587

Yamazaki D, Tabara Y, Kita S, Hanada H, Komazaki S, Naitou D, Mishima A, Nishi M, Yamamura H, Yamamoto S,

Kakizawa S, Miyachi H, Yamamoto S, Miyata T, Kawano Y, Kamide K, Ogihara T, Hata A, Umemura S, Soma M,

et al. 2011. TRIC-­A channels in vascular smooth muscle contribute to blood pressure maintenance. Cell

Metabolism 14:231–241. DOI: https://doi.org/10.1016/j.cmet.2011.05.011, PMID: 21803293

Yasoda A., Ogawa Y, Suda M, Tamura N, Mori K, Sakuma Y, Chusho H, Shiota K, Tanaka K, Nakao K. 1998.

Natriuretic Peptide Regulation of Endochondral Ossification. Journal of Biological Chemistry 273:11695–

11700. DOI: https://doi.org/10.1074/jbc.273.19.11695, PMID: 9565590

Yasoda A, Komatsu Y, Chusho H, Miyazawa T, Ozasa A, Miura M, Kurihara T, Rogi T, Tanaka S, Suda M, Tamura N,

Ogawa Y, Nakao K. 2004. Overexpression of CNP in chondrocytes rescues achondroplasia through a MAPK-­

dependent pathway. Nature Medicine 10:80–86. DOI: https://doi.org/10.1038/nm971, PMID: 14702637

Zhao C, Ichimura A, Qian N, Iida T, Yamazaki D, Noma N, Asagiri M, Yamamoto K, Komazaki S, Sato C,

Aoyama F, Sawaguchi A, Kakizawa S, Nishi M, Takeshima H. 2016. Mice lacking the intracellular cation channel

TRIC-­B have compromised collagen production and impaired bone mineralization. Science Signaling 9:ra49.

DOI: https://doi.org/10.1126/scisignal.aad9055, PMID: 27188440

Zois NE, Bartels ED, Hunter I, Kousholt BS, Olsen LH, Goetze JP. 2014. Natriuretic peptides in cardiometabolic

regulation and disease. Nature Reviews. Cardiology 11:403–412. DOI: https://doi.org/10.1038/nrcardio.2014.​

64, PMID: 24820868

Miyazaki, Ichimura, et al. eLife 2022;11:e71931. DOI: https://doi.org/10.7554/eLife.71931

23 of 23

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