Top

Published in:

08-07-2023 | Invited Review

Resistance exercise stress: theoretical mechanisms for growth hormone processing and release from the anterior pituitary somatotroph

Authors: Wesley C. Hymer, William J. Kraemer

Published in: European Journal of Applied Physiology | Issue 9/2023

Abstract

Heavy resistance exercise (HRE) is the most effective method for inducing muscular hypertrophy and stimulating anabolic hormones, including growth hormone, into the blood. In this review, we explore possible mechanisms within the GH secretory pathway of the pituitary somatotroph, which are likely to modulate the flow of hormone synthesis and packaging as it is processed prior to exocytosis. Special emphasis is placed on the secretory granule and its possible role as a signaling hub. We also review data that summarize how HRE affects the quality and quantity of the secreted hormone. Finally, these pathway mechanisms are considered in the context of heterogeneity of the somatotroph population in the anterior pituitary.

Available only for authorised users

Ariyasu D, Yoshida H, Yamada M, Hasegawa Y (2013) Endoplasmic reticulum stress and apoptosis contribute to the pathogenesis of dominantly inherited isolated GH deficiency due to GH1 gene splice site mutations. Endocrinology 154(9):3228–3239. https://doi.org/10.1210/en.2013-1249CrossRefPubMed

Asai S, Moravcova J, Zakova L, Selicharova I, Hadravova R, Brzozowski AM, Novacek J, Jiracek J (2022) Characterization of insulin crystalline form in isolated beta-cell secretory granules. Open Biol 12(12):220322. https://doi.org/10.1098/rsob.220322CrossRefPubMedPubMedCentral

Back N, Rajagopal C, Mains RE, Eipper BA (2010) Secretory granule membrane protein recycles through multivesicular bodies. Traffic 11(7):972–986. https://doi.org/10.1111/j.1600-0854.2010.01066.xCrossRefPubMedPubMedCentral

Baumann G (1991) Growth hormone heterogeneity: genes, isohormones, variants, and binding proteins. Endocr Rev 12(4):424–449. https://doi.org/10.1210/edrv-12-4-424CrossRefPubMed

Ben-Zeev G, Telias M, Nussinovitch I (2010) Lysophospholipids modulate voltage-gated calcium channel currents in pituitary cells; effects of lipid stress. Cell Calcium 47(6):514–524. https://doi.org/10.1016/j.ceca.2010.04.006CrossRefPubMed

Bonnefont X, Lacampagne A, Sanchez-Hormigo A, Fino E, Creff A, Mathieu MN, Smallwood S, Carmignac D, Fontanaud P, Travo P, Alonso G, Courtois-Coutry N, Pincus SM, Robinson IC, Mollard P (2005) Revealing the large-scale network organization of growth hormone-secreting cells. Proc Natl Acad Sci USA 102(46):16880–16885. https://doi.org/10.1073/pnas.0508202102CrossRefPubMedPubMedCentral

Bonnemaison ML, Eipper BA, Mains RE (2013) Role of adaptor proteins in secretory granule biogenesis and maturation. Front Endocrinol (lausanne) 4:101. https://doi.org/10.3389/fendo.2013.00101CrossRefPubMed

Cochilla AJ, Angleson JK, Betz WJ (2000) Differential regulation of granule-to-granule and granule-to-plasma membrane fusion during secretion from rat pituitary lactotrophs. J Cell Biol 150(4):839–848. https://doi.org/10.1083/jcb.150.4.839CrossRefPubMedPubMedCentral

Cool DR, Normant E, Shen F, Chen HC, Pannell L, Zhang Y, Loh YP (1997) Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88(1):73–83. https://doi.org/10.1016/s0092-8674(00)81860-7CrossRefPubMed

Cunningham BC, Mulkerrin MG, Wells JA (1991) Dimerization of human growth hormone by zinc. Science 253(5019):545–548. https://doi.org/10.1126/science.1907025CrossRefPubMed

Dannies PS (2012) Prolactin and growth hormone aggregates in secretory granules: the need to understand the structure of the aggregate. Endocr Rev 33(2):254–270. https://doi.org/10.1210/er.2011-1002CrossRefPubMed

Davies NG, Abbott S, Barnard RC, Jarvis CI, Kucharski AJ, Munday JD, Pearson CAB, Russell TW, Tully DC, Washburne AD, Wenseleers T, Gimma A, Waites W, Wong KLM, van Zandvoort K, Silverman JD, Group CC-W, Consortium C-GU, Diaz-Ordaz K, Keogh R, Eggo RM, Funk S, Jit M, Atkins KE, Edmunds WJ (2021) Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science. https://doi.org/10.1126/science.abg3055CrossRefPubMedPubMedCentral

Dehkhoda F, Lee CMM, Medina J, Brooks AJ (2018) The growth hormone receptor: mechanism of receptor activation, cell signaling, and physiological aspects. Front Endocrinol (lausanne) 9:35. https://doi.org/10.3389/fendo.2018.00035CrossRefPubMed

Eipper BA, Green CB, Mains RE (1992a) Expression of prohormone processing enzymes in neuroendocrine and non-neuroendocrine cells. J Natl Cancer Inst Monogr 13:163–168

Eipper BA, Stoffers DA, Mains RE (1992b) The biosynthesis of neuropeptides: peptide alpha-amidation. Annu Rev Neurosci 15:57–85. https://doi.org/10.1146/annurev.ne.15.030192.000421CrossRefPubMed

El Meskini R, Mains RE, Eipper BA (2000) Cell type-specific metabolism of peptidylglycine alpha-amidating monooxygenase in anterior pituitary. Endocrinology 141(8):3020–3034. https://doi.org/10.1210/endo.141.8.7620CrossRefPubMed

El Meskini R, Galano GJ, Marx R, Mains RE, Eipper BA (2001) Targeting of membrane proteins to the regulated secretory pathway in anterior pituitary endocrine cells. J Biol Chem 276(5):3384–3393. https://doi.org/10.1074/jbc.M008062200CrossRefPubMed

Farhan H, Rabouille C (2011) Signalling to and from the secretory pathway. J Cell Sci 124(Pt 2):171–180. https://doi.org/10.1242/jcs.076455CrossRefPubMed

Farrington M, Hymer WC (1990) Growth hormone aggregates in the rat adenohypophysis. Endocrinology 126(3):1630–1638. https://doi.org/10.1210/endo-126-3-1630CrossRefPubMed

Fass D, Thorpe C (2018) Chemistry and enzymology of disulfide cross-linking in proteins. Chem Rev 118(3):1169–1198. https://doi.org/10.1021/acs.chemrev.7b00123CrossRefPubMed

Ferraro F, Eipper BA, Mains RE (2005) Retrieval and reuse of pituitary secretory granule proteins. J Biol Chem 280(27):25424–25435. https://doi.org/10.1074/jbc.M414156200CrossRefPubMed

Grindeland RE, Kraemer WJ, Hymer WC (2017) Two types of rat pituitary somatotrophs secrete growth hormone with different biological and immunological profiles. Growth Horm IGF Res 36:52–56. https://doi.org/10.1016/j.ghir.2017.09.001CrossRefPubMed

Hatfield DL, Kraemer WJ, Volek JS, Nindl BC, Caldwell LK, Vingren JL, Newton RU, Hakkinen K, Lee EC, Maresh CM, Hymer WC (2021) Hormonal stress responses of growth hormone and insulin-like growth factor-I in highly resistance trained women and men. Growth Horm IGF Res 59:101407. https://doi.org/10.1016/j.ghir.2021.101407CrossRefPubMed

Hopkins CR, Farquhar MG (1973) Hormone secretion by cells dissociated from rat anterior pituitaries. J Cell Biol 59(2 Pt 1):276–303. https://doi.org/10.1083/jcb.59.2.276CrossRefPubMedPubMedCentral

Hymer WC, Kraicer J, Bencosme SA, Haskill JS (1972) Separation of somatotrophs from the rat adenohypophysis by velocity and density gradient centrifugation. Proc Soc Exp Biol Med 141(3):966–973. https://doi.org/10.3181/00379727-141-36912CrossRefPubMed

Hymer W, Kirshnan K, Kraemer W, Welsch J, Lanham W (2000) Mammalian pituitary growth hormone: applications of free flow electrophoresis. Electrophoresis 21(2):311–317. https://doi.org/10.1002/(SICI)1522-2683(20000101)21:2%3c311::AID-ELPS311%3e3.0.CO;2-8CrossRefPubMed

Hymer WC, Kraemer WJ, Nindl BC, Marx JO, Benson DE, Welsch JR, Mazzetti SA, Volek JS, Deaver DR (2001) Characteristics of circulating growth hormone in women after acute heavy resistance exercise. Am J Physiol Endocrinol Metab 281(4):E878-887. https://doi.org/10.1152/ajpendo.2001.281.4.E878CrossRefPubMed

Hymer WC, Kennett MJ, Maji SK, Gosselink KL, McCall GE, Grindeland RE, Post EM, Kraemer WJ (2020) Bioactive growth hormone in humans: controversies, complexities and concepts. Growth Horm IGF Res 50:9–22. https://doi.org/10.1016/j.ghir.2019.11.003CrossRefPubMed

Jacob RS, Das S, Ghosh S, Anoop A, Jha NN, Khan T, Singru P, Kumar A, Maji SK (2016) Amyloid formation of growth hormone in presence of zinc: relevance to its storage in secretory granules. Sci Rep 6:23370. https://doi.org/10.1038/srep23370CrossRefPubMedPubMedCentral

Jiang Y, Neti SS, Sitarik I, Pradhan P, To P, Xia Y, Fried SD, Booker SJ, O’Brien EP (2023) How synonymous mutations alter enzyme structure and function over long timescales. Nat Chem 15(3):308–318. https://doi.org/10.1038/s41557-022-01091-zCrossRefPubMed

Kannenberg K, Wittekindt NE, Tippmann S, Wolburg H, Ranke MB, Binder G (2007) Mutant and misfolded human growth hormone is rapidly degraded through the proteasomal degradation pathway in a cellular model for isolated growth hormone deficiency type II. J Neuroendocrinol 19(11):882–890. https://doi.org/10.1111/j.1365-2826.2007.01602.xCrossRefPubMed

Kilic G, Angleson JK, Cochilla AJ, Nussinovitch I, Betz WJ (2001) Sustained stimulation of exocytosis triggers continuous membrane retrieval in rat pituitary somatotrophs. J Physiol 532(Pt 3):771–783. https://doi.org/10.1111/j.1469-7793.2001.0771e.xCrossRefPubMedPubMedCentral

Kraemer WJ, Ratamess NA (2004) Fundamentals of resistance training: progression and exercise prescription. Med Sci Sports Exerc 36(4):674–688. https://doi.org/10.1249/01.mss.0000121945.36635.61CrossRefPubMed

Kraemer WJ, Marchitelli L, Gordon SE, Harman E, Dziados JE, Mello R, Frykman P, McCurry D, Fleck SJ (1990) Hormonal and growth factor responses to heavy resistance exercise protocols. J Appl Physiol (1985) 69(4):1442–1450. https://doi.org/10.1152/jappl.1990.69.4.1442CrossRefPubMed

Kraemer WJ, Gordon SE, Fleck SJ, Marchitelli LJ, Mello R, Dziados JE, Friedl K, Harman E, Maresh C, Fry AC (1991) Endogenous anabolic hormonal and growth factor responses to heavy resistance exercise in males and females. Int J Sports Med 12(2):228–235. https://doi.org/10.1055/s-2007-1024673CrossRefPubMed

Kraemer WJ, Fleck SJ, Dziados JE, Harman EA, Marchitelli LJ, Gordon SE, Mello R, Frykman PN, Koziris LP, Triplett NT (1993) Changes in hormonal concentrations after different heavy-resistance exercise protocols in women. J Appl Physiol (1985) 75(2):594–604. https://doi.org/10.1152/jappl.1993.75.2.594CrossRefPubMed

Kraemer WJ, Nindl BC, Marx JO, Gotshalk LA, Bush JA, Welsch JR, Volek JS, Spiering BA, Maresh CM, Mastro AM, Hymer WC (2006) Chronic resistance training in women potentiates growth hormone in vivo bioactivity: characterization of molecular mass variants. Am J Physiol Endocrinol Metab 291(6):E1177-1187. https://doi.org/10.1152/ajpendo.00042.2006CrossRefPubMed

Kraemer WJ, Flanagan SD, Volek JS, Nindl BC, Vingren JL, Dunn-Lewis C, Comstock BA, Hooper DR, Szivak TK, Looney DP, Maresh CM, Hymer WC (2013) Resistance exercise induces region-specific adaptations in anterior pituitary gland structure and function in rats. J Appl Physiol (1985) 115(11):1641–1647. https://doi.org/10.1152/japplphysiol.00687.2013CrossRefPubMed

Kraemer WJ, Ratamess NA, Nindl BC (2017) Recovery responses of testosterone, growth hormone, and IGF-1 after resistance exercise. J Appl Physiol 122(3):549–558. https://doi.org/10.1152/japplphysiol.00599.2016CrossRefPubMed

Kraemer WJ, Caldwell LK, Post EM, Beeler MK, Dickerson RM, Kennett MJ, Volek JS, Maresh CM, Hymer WC (2020a) Recovery using “float” from high intensity stress on growth hormone-like molecules in resistance trained men. Growth Horm IGF Res 55:101355. https://doi.org/10.1016/j.ghir.2020.101355CrossRefPubMed

Kraemer WJ, Ratamess NA, Hymer WC, Nindl BC, Fragala MS (2020b) Growth hormone(s), testosterone, insulin-like growth factors, and cortisol: roles and integration for cellular development and growth with exercise. Front Endocrinol (lausanne) 11:33. https://doi.org/10.3389/fendo.2020.00033CrossRefPubMed

Lafont C, Desarmenien MG, Cassou M, Molino F, Lecoq J, Hodson D, Lacampagne A, Mennessier G, El Yandouzi T, Carmignac D, Fontanaud P, Christian H, Coutry N, Fernandez-Fuente M, Charpak S, Le Tissier P, Robinson IC, Mollard P (2010) Cellular in vivo imaging reveals coordinated regulation of pituitary microcirculation and GH cell network function. Proc Natl Acad Sci USA 107(9):4465–4470. https://doi.org/10.1073/pnas.0902599107CrossRefPubMedPubMedCentral

Le Tissier PR, Hodson DJ, Lafont C, Fontanaud P, Schaeffer M, Mollard P (2012) Anterior pituitary cell networks. Front Neuroendocrinol 33(3):252–266. https://doi.org/10.1016/j.yfrne.2012.08.002CrossRefPubMed

Levine CG, Mitra D, Sharma A, Smith CL, Hegde RS (2005) The efficiency of protein compartmentalization into the secretory pathway. Mol Biol Cell 16(1):279–291. https://doi.org/10.1091/mbc.e04-06-0508CrossRefPubMedPubMedCentral

Lorenson LG, Dunn MA, Blevins RD (1986) In vitro modulation of growth hormone release from bovine pituitary granules by zinc and adenosine triphosphate. Endocrinology 118(1):344–350

Lukaszewska J, Biczowa B, Bobilewicz D, Wilk M, Obuchowicz-Fidelus B (1976) Effect of physical exercise on plasma cortisol and growth hormone levels in young weight lifters. Endokrynol Pol 27(2):149–157PubMed

Maji SK, Schubert D, Rivier C, Lee S, Rivier JE, Riek R (2008) Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol 6(2):e17. https://doi.org/10.1371/journal.pbio.0060017CrossRefPubMedPubMedCentral

Maji SK, Wang L, Greenwald J, Riek R (2009) Structure-activity relationship of amyloid fibrils. FEBS Lett 583(16):2610–2617. https://doi.org/10.1016/j.febslet.2009.07.003CrossRefPubMed

McCall GE, Goulet C, Grindeland RE, Hodgson JA, Bigbee AJ, Edgerton VR (1997) Bed rest suppresses bioassayable growth hormone release in response to muscle activity. J Appl Physiol (1985) 83(6):2086–2090. https://doi.org/10.1152/jappl.1997.83.6.2086CrossRefPubMed

Mehra S, Gadhe L, Bera R, Sawner AS, Maji SK (2021) Structural and functional insights into alpha-synuclein fibril polymorphism. Biomolecules. https://doi.org/10.3390/biom11101419CrossRefPubMedPubMedCentral

Michael DJ, Ritzel RA, Haataja L, Chow RH (2006) Pancreatic beta-cells secrete insulin in fast- and slow-release forms. Diabetes 55(3):600–607. https://doi.org/10.2337/diabetes.55.03.06.db05-1054CrossRefPubMed

Mullis PE, Deladoey J, Dannies PS (2002) Molecular and cellular basis of isolated dominant-negative growth hormone deficiency, IGHD type II: insights on the secretory pathway of peptide hormones. Horm Res 58(2):53–66. https://doi.org/10.1159/000064663CrossRefPubMed

Nakagawa J, Mori H, Maeda T, Matsuo T, Okada Y (1995) Dynamics of secretory granules in somatotrophs of rats after stimulation with growth hormone-releasing factor: a stereological analysis. Cell Tissue Res 282(3):493–501. https://doi.org/10.1007/BF00318881CrossRefPubMed

Olson KC, Fenno J, Lin N, Harkins RN, Snider C, Kohr WH, Ross MJ, Fodge D, Prender G, Stebbing N (1981) Purified human growth hormone from E. coli is biologically active. Nature 293(5831):408–411. https://doi.org/10.1038/293408a0CrossRefPubMed

Palivec V, Viola CM, Kozak M, Ganderton TR, Krizkova K, Turkenburg JP, Haluskova P, Zakova L, Jiracek J, Jungwirth P, Brzozowski AM (2017) Computational and structural evidence for neurotransmitter-mediated modulation of the oligomeric states of human insulin in storage granules. J Biol Chem 292(20):8342–8355. https://doi.org/10.1074/jbc.M117.775924CrossRefPubMedPubMedCentral

Pierce JR, Martin BJ, Rarick KR, Alemany JA, Staab JS, Kraemer WJ, Hymer WC, Nindl BC (2020) Growth hormone and insulin-like growth factor-I molecular weight isoform responses to resistance exercise are sex-dependent. Front Endocrinol (lausanne) 11:571. https://doi.org/10.3389/fendo.2020.00571CrossRefPubMed

Protter DSW, Parker R (2016) Principles and properties of stress granules. Trends Cell Biol 26(9):668–679. https://doi.org/10.1016/j.tcb.2016.05.004CrossRefPubMedPubMedCentral

Rabdano SO, Izmailov SA, Luzik DA, Groves A, Podkorytov IS, Skrynnikov NR (2017) Onset of disorder and protein aggregation due to oxidation-induced intermolecular disulfide bonds: case study of RRM2 domain from TDP-43. Sci Rep 7(1):11161. https://doi.org/10.1038/s41598-017-10574-wCrossRefPubMedPubMedCentral

Rajagopal C, Mains RE, Eipper BA (2012) Signaling from the secretory granule to the nucleus. Crit Rev Biochem Mol Biol 47(4):391–406. https://doi.org/10.3109/10409238.2012.694845CrossRefPubMedPubMedCentral

Reck J, Beuret N, Demirci E, Prescianotto-Baschong C, Spiess M (2022) Small disulfide loops in peptide hormones mediate self-aggregation and secretory granule sorting. Life Sci Alliance. https://doi.org/10.26508/lsa.202101279CrossRefPubMedPubMedCentral

Sanchez-Cardenas C, Fontanaud P, He Z, Lafont C, Meunier AC, Schaeffer M, Carmignac D, Molino F, Coutry N, Bonnefont X, Gouty-Colomer LA, Gavois E, Hodson DJ, Le Tissier P, Robinson IC, Mollard P (2010) Pituitary growth hormone network responses are sexually dimorphic and regulated by gonadal steroids in adulthood. Proc Natl Acad Sci USA 107(50):21878–21883. https://doi.org/10.1073/pnas.1010849107CrossRefPubMedPubMedCentral

Sander M, Wu Z, Strasburger CJ (2020) Short stature explained by dimerization of human growth hormone induced by a p.C53S point mutation. J Biol Chem 295(15):4893–4901. https://doi.org/10.1074/jbc.RA119.009101CrossRefPubMedPubMedCentral

Shafqat J, Melles E, Sigmundsson K, Johansson BL, Ekberg K, Alvelius G, Henriksson M, Johansson J, Wahren J, Jornvall H (2006) Proinsulin C-peptide elicits disaggregation of insulin resulting in enhanced physiological insulin effects. Cell Mol Life Sci 63(15):1805–1811. https://doi.org/10.1007/s00018-006-6204-6CrossRefPubMedPubMedCentral

Skierska E, Ustupska J, Biczowa B, Lukaszewska J (1976) Effect of physical exercise on plasma cortisol, testosterone and growth hormone levels in weight lifters. Endokrynol Pol 27(2):159–165PubMed

Snyder G, Hymer WC, Snyder J (1977) Functional heterogeneity in somatotrophs isolated from the rat anterior pituitary. Endocrinology 101(3):788–799. https://doi.org/10.1210/endo-101-3-788CrossRefPubMed

Sontag EM, Samant RS, Frydman J (2017) Mechanisms and functions of spatial protein quality control. Annu Rev Biochem 86:97–122. https://doi.org/10.1146/annurev-biochem-060815-014616CrossRefPubMed

Stachura ME, Costoff A, Tyler JM (1986) Structural correlates of stimulated and inhibited secretion: electron microscopic observations of somatotrophs in perifused rat pituitary. Neuroendocrinology 42(5):383–391. https://doi.org/10.1159/000124476CrossRefPubMed

Suckale J, Solimena M (2010) The insulin secretory granule as a signaling hub. Trends Endocrinol Metab 21(10):599–609. https://doi.org/10.1016/j.tem.2010.06.003CrossRefPubMed

Trifunovic S, Lakic I, Vujovic P, Jevdjovic T, Sosic-Jurjevic B, Milosevic V, Djordjevic J (2019) Morphofunctional parameters of rat somatotrophes after acute and repeated immobilization or restraint stress. Acta Histochem 121(1):29–34. https://doi.org/10.1016/j.acthis.2018.10.003CrossRefPubMed

Vanhelder WP, Goode RC, Radomski MW (1984) Effect of anaerobic and aerobic exercise of equal duration and work expenditure on plasma growth hormone levels. Eur J Appl Physiol Occup Physiol 52(3):255–257. https://doi.org/10.1007/BF01015205CrossRefPubMed

Walsh IM, Bowman MA, Soto Santarriaga IF, Rodriguez A, Clark PL (2020) Synonymous codon substitutions perturb cotranslational protein folding in vivo and impair cell fitness. Proc Natl Acad Sci USA 117(7):3528–3534. https://doi.org/10.1073/pnas.1907126117CrossRefPubMedPubMedCentral

Wandinger-Ness A, Zerial M (2014) Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol 6(11):a022616. https://doi.org/10.1101/cshperspect.a022616CrossRefPubMedPubMedCentral

Zheng Z, Shang Y, Tao J, Zhang J, Sha B (2019) Endoplasmic reticulum stress signaling pathways: activation and diseases. Curr Protein Pept Sci 20(9):935–943. https://doi.org/10.2174/1389203720666190621103145CrossRefPubMed

Title: Resistance exercise stress: theoretical mechanisms for growth hormone processing and release from the anterior pituitary somatotroph
Authors: Wesley C. Hymer
William J. Kraemer
Publication date: 08-07-2023
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 9/2023
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-023-05263-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Resistance exercise stress: theoretical mechanisms for growth hormone processing and release from the anterior pituitary somatotroph

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2023

Evaluation of a preemptive intervention regimen with hesperidin methyl chalcone in delayed-onset muscle soreness in young adults: a randomized, double-blinded, and placebo-controlled trial study

Repeated cold-water immersion improves autonomic cardiac modulation following five sessions of high-intensity interval exercise

Carbohydrate, but not fat, oxidation is reduced during moderate-intensity exercise performed in 33 vs. 18 °C at matched heart rates

Effects on hemodynamic enhancement and discomfort of a new textile electrode integrated in a sock during calf neuromuscular electrical stimulation

Eccentric exercise 24 h prior to hypobaric decompression increases decompression strain

Adaptability of the load sharing between the longissimus and components of the multifidus muscle during isometric trunk extension in healthy individuals