Stretching mechanotransduction from the lung to the lab: Approaches and physiological relevance in drug discovery

Assay and Drug Development Technologies

Volumn 10, Issue 2, 2012, Pages 137-147

  Schmitt, Sarah ^a   Hendricks, Peter ^b   Weir, Josh ^b   Somasundaram, Raj ^b   Sittampalam, G Sitta ^b,c   Nirmalanandhan, Victor Sanjit ^b,c  

^a University of Kansas   (United States)

^b UNIVERSITY OF KANSAS CANCER CENTER   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ANTINEOPLASTIC AGENT; CISPLATIN; DOXORUBICIN; MITOTIC INHIBITOR; PACLITAXEL; PHOSPHOLIPASE C INHIBITOR; PROTEIN KINASE C INHIBITOR; UNCLASSIFIED DRUG; UO 126;

BIOREACTOR; BREATHING; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; DRUG MECHANISM; DRUG SCREENING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG; LUNG DEVELOPMENT; LUNG INJURY; MECHANOTRANSDUCTION; NONHUMAN; REVIEW;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; HUMANS; LUNG; MECHANOTRANSDUCTION, CELLULAR; PULMONARY STRETCH RECEPTORS; RESPIRATORY MECHANICS; STRESS, MECHANICAL;

EID: 84859865740     PISSN: 1540658X     EISSN: 15578127     Source Type: Journal    
DOI: 10.1089/adt.2011.418     Document Type: Review

References (105)

1. Wyszogrodski I, Taeusch HW, Kyeiaboagye K, Avery ME: Mechanical regulation of alveolar surfactant in adult cats-effects of hyperventilation and endexpiratory pressure in vivo. Chest 1975;67:S15-S16
2. Alcorn D, Adamson TM, Lambert TF, Maloney JE, Ritchie BC, Robinson PM: Morphological effects of chronic tracheal ligation and drainage in fetal lamb lung. J Anat 1977;123:649-660
3. Wigglesworth JS, Desai R: Effects on lung growth of cervical cord section in the rabbit fetus. Early Hum Develop 1979;3:51-65
4. Liu MY, Tanswell AK, Post M: Mechanical force-induced signal transduction in lung cells. Am J Physiol Lung Cell Mol Physiol 1999;277:L667-L683
5. Liu MY, Post M: Invited review: mechanochemical signal transduction in the fetal lung. J Appl Physiol 2000;89:2078-2084
6. Edwards YS: Stretch stimulation: its effects on alveolar type II cell function in the lung. Comp Biochem Physiol A Mol Integr Physiol 2001;129:245-260
7. Maloney JE, Adamson TM, Brodecky V, Cranage S, Lambert TF, Ritchie BC: Diaphragmatic activity and lung liquid flow in unanesthetized fetal sheep. J Appl Physiol 1975;39:423-428
8. Fewell JE, Hislop AA, Kitterman JA, Johnson P: Effect of tracheostomy on lung development in fetal lambs. J Appl Physiol 1983;55:1103-1108
9. Moessinger AC, Harding R, Adamson TM, Singh M, Kiu GT: Role of lung fluid volume in growth and maturation of the fetal sheep lung. J Clin Invest 1990;86:1270-1277
10. de Lorimier AA, Tierney DF, Parker HR: Hypoplastic lungs in fetal lambs with surgically produced congenital diaphragmatic hernia. Surgery 1967;62:12-17
11. Pringle KC, Turner JW, Schofield JC, Soper RT: Creation and repair of diaphragmatic-hernia in the fetal lamb-lung development and morphology. J Pediatr Surg 1984;19:131-140
12. Alcorn D, Adamson TM, Maloney JE, Robinson PM: Morphological effects of chronic bilateral phrenectomy or vagotomy in the fetal lamb lung. J Anat 1980;130:683-695
13. Fewell JE, Lee CC, Kitterman JA: Effects of phrenic-nerve section on the respiratory system of fetal lambs. J Appl Physiol 1981;51:293-297
14. Kumar S, Weaver V: Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 2009;28:113-127
15. Tschumperlin DJ, Margulies SS: Equibiaxial deformation-induced injury of alveolar epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 1998; 275:L1173-L1183
16. Tschumperlin DJ, Oswari J, Margulies SS: Deformation-induced injury of alveolar epithelial cells-effect of frequency, duration, and amplitude. Am J Respir Crit Care Med 2000;162:357-362
17. McAdams RM, Mustafa SB, Shenberger JS, Dixon PS, Henson BM, DiGeronimo RJ: Cyclic stretch attenuates effects of hyperoxia on cell proliferation and viability in human alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006;291:L166-L174
18. Geddes-Klein DM, Schiffman KB, Meaney DF: Mechanisms and consequences of neuronal stretch injury in vitro differ with the model of trauma. J Neurotrauma 2006;23:193-204
19. Kato T, Ishiguro N, Iwata H, Kojima T, Ito T, Naruse K: Up-regulation of COX2 expression by uni-axial cyclic stretch in human lung fibroblast cells. Biochem Biophys Res Commun 1998;244:615-619
20. Hu XB, Zhang YY, Cheng DY, et al.: Mechanical stress upregulates intercellular adhesion molecule-1 in pulmonary epithelial cells. Respiration 2008;76:344-350
21. Mijailovich SM, Stamenovic D, Brown R, Leith DE, Fredberg JJ: Dynamic moduli of rabbit lung-tissue and pigeon ligamentum propatagiale undergoing uniaxial cyclic loading. J Appl Physiol 1994;76:773-782
22. Banes A, Gilbert J, Taylor D, Monbureau O: A new vacuum-operated stressproviding instrument that applies static or variable duration cyclic tension or compression to cells in vitro. J Cell Sci 1985;75:35-42
23. Dassow C, Wiechert L, Martin C, et al.: Biaxial distension of precision-cut lung slices. J Appl Physiol 2010;108:713-721
24. Gorfien SF, Winston FK, Thibault LE, Macarak EJ: Effects of biaxial deformation on pulmonary-artery endothelial-cells. J Cell Physiol 1989;139:492-500
25. Williams JL, Chen JH, Belloli DM: Strain fields on cell stressing devices employing clamped circular elastic diaphragms as substrates. J Biomech Eng 1992;114:377-384
26. Brighton CT, Strafford B, Gross SB, Leatherwood DF, Williams JL, Pollack SR: The proliferative and synthetic response of isolated calvarial bone-cells of rats to cyclic biaxial mechanical strain. J Bone Joint Surg Am 1991;73A:320-331
27. Hasegawa S, Sato S, Saito S, Suzuki Y, Brunette DM: Mechanical stretching increases the number of cultured bone-cells synthesizing DNA and alters their pattern of protein-synthesis. Calcif Tissue Int 1985;37:431-436
28. Vandenburgh HH: A computerized mechanical cell stimulator for tissueculture- effects on skeletal-muscle organogenesis. In Vitro Cell Dev Biol 1988;24:609-619
29. Sanchez-Esteban J, Cicchiello LA, Wang YL, et al.: Mechanical stretch promotes alveolar epithelial type II cell differentiation. J Appl Physiol 2001;91:589-595
30. Sanchez-Esteban J, Wang Y, Gruppuso PA, Rubin LP: Mechanical stretch induces fetal type II cell differentiation via an epidermal growth factor receptor-extracellular-regulated protein kinase signaling pathway. Am J Respir Cell Mol Biol 2004;30:76-83
31. Wang YL, Maciejewski BS, Lee N, et al.: Strain-induced fetal type II epithelial cell differentiation is mediated via cAMP-PKA-dependent signaling pathway. Am J Physiol Lung Cell Mol Physiol 2006;291:L820-L827
32. Smith PG, Janiga KE, Bruce MC: Strain increases airway smooth-muscle cellproliferation. Am J Respir Cell Mol Biol 1994;10:85-90
33. Chess PR, Toia L, Finkelstein JN: Mechanical strain-induced proliferation and signaling in pulmonary epithelial H441 cells. Am J Physiol Lung Cell Mol Physiol 2000;279:L43-L51
34. Chaturvedi LS, Marsh HM, Basson MD: Src and focal adhesion kinase mediate mechanical strain-induced proliferation and ERK1/2 phosphorylation in human H441 pulmonary epithelial cells. Am J Physiol Cell Physiol 2007;292:C1701-1713
35. dos Santos CC, Han B, Andrade CF, et al.: DNA microarray analysis of gene expression in alveolar epithelial cells in response to TNFa, LPS, and cyclic stretch. Physiol Genomics 2004;19:331-342
36. Copland IB, Post M: Stretch-activated signaling pathways responsible for early response gene expression in fetal lung epithelial cells. J Cell Physiol 2007;210:133-143
37. Sanchez-Esteban J, Tsai SW, Sang JB, Qin J, Torday JS, Rubin LP: Effects of mechanical forces on lung-specific gene expression. Am J Med Sci 1998;316:200-204
38. Kamotani Y, Bersano-Begey T, Kato N, et al.: Individually programmable cell stretching microwell arrays actuated by a Braille display. Biomaterials 2008; 29:2646-2655
39. Moraes C, Chen JH, Sun Y, Simmons CA: Microfabricated arrays for highthroughput screening of cellular response to cyclic substrate deformation. Lab Chip 2010;10:227-234
40. Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE: Reconstituting organ-level lung functions on a chip. Science 2010;328:1662-1668
41. Chen C, Krishnan R, Zhou EH, et al.: Fluidization and resolidification of the human bladder smooth muscle cell in response to transient stretch. PLoS One 2010;5:e12035
42. Krishnan R, Park CY, Lin YC, et al.: Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness. PLoS One 2009;4:e5486
43. Mih JD, Sharif AS, Liu F, Marinkovic A, Symer MM, Tschumperlin DJ:A multiwell platform for studying stiffness-dependent cell biology. PLoS One 2011;6:e19929
44. Ingber DE: Tensegrity: the architectural basis of cellular mechanotransduction. Ann Rev Physiol 1997;59:575-599
45. Ingber DE: Tensegrity II: How structural networks influence cellular information processing networks. J Cell Sci 2003;116:1397-1408
46. Jaalouk DE, Lammerding J: Mechanotransduction gone awry. Nat Rev Mol Cell Biol 2009;10:63-73
47. Butcher DT, Alliston T, Weaver VM: A tense situation: forcing tumour progression. Nat Rev Cancer 2009;9:108-122
48. Kitterman JA: The effects of mechanical forces on fetal lung growth. Clin Perinatol 1996;23:727-740
49. Correa-Meyer E, Pesce L, Guerrero C, Sznajder JI: Mechanotransduction in the lung-cyclic stretch activates ERK1/2 via G proteins and EGFR in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002;282:L883-L891
50. Gutierrez JA, Gonzalez RF, Dobbs LG: Mechanical distension modulates pulmonary alveolar epithelial phenotypic expression in vitro. Am J Physiol Lung Cell Mol Physiol 1998;274:L196-L202
51. Chess PR, O'Reilly MA, Sachs F, Finkelstein JN: Reactive oxidant and p42/ 44 MAP kinase signaling is necessary for mechanical strain-induced proliferation in pulmonary epithelial cells. J Appl Physiol 2005;99:1226-1232
52. Chapman GB, Durante W, Hellums JD, Schafer AI: Physiological cyclic stretch causes cell cycle arrest in cultured vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2000;278:H748-754
53. Sanchez-Esteban J, Wang YL, Cicchiello LA, Rubin LP: Pre- and postnatal lung development, maturation, and plasticity-cyclic mechanical stretch inhibits cell proliferation and induces apoptosis in fetal rat lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2002;282:L448-L456
54. Bishop JE, Mitchell JJ, Absher PM, et al.: Cyclic mechanical deformation stimulates human lung fibroblast proliferation and autocrine growth-factor activity. Am J Respir Cell Mol Biol 1993;9:126-133
55. Liu M, Skinner SJM, Xu J, Han RNN, Tanswell AK, Post M: Stimulation of fetalrat lung-cell proliferation invitro by mechanical stretch. Am J Physiol 1992; 263:L376-L383
56. Liu MY, Xu JG, Liu J, Kraw ME, Tanswell AK, Post M: Mechanical strainenhanced fetal lung-cell proliferation is mediated by phospholipase-c and phospholipase-d and protein-kinase-c. Am J Physiol Lung Cell Mol Physiol 1995;268:L729-L738
57. Liu M, Xu J, Souza P, Tanswell B, Tanswell AK, Post M: The effect of mechanical strain on fetal rat lung cell proliferation: comparison of two- and three-dimensional culture systems. In Vitro Cell Dev Biol Anim 1995;31: 858-866
58. Xu J, Liu MY, Tanswell AK, Post M: Mesenchymal determination of mechanical strain-induced fetal lung cell proliferation. Am J Physiol Lung Cell Mol Physiol 1998;275:L545-L550
59. Edwards YS, Sutherland LM, Power JHT, Nicholas TE, Murray AW: Cyclic stretch induces both apoptosis and secretion in rat alveolar type II cells. FEBS Lett 1999;448:127-130
60. Yamamoto H, Teramoto H, Uetani K, Igawa K, Shimizu E: Stretch induces a growth factor in alveolar cells via protein kinase. Respir Physiol 2001;127: 105-111
61. Liu M, Liu J, Buch S, Tanswell AK, Post M: Antisense oligonucleotides for PDGF-B and its receptor inhibit mechanical strain-induced fetal lung cell growth. Am J Physiol Lung Cell Mol Physiol 1995;269:L178-184
62. Quinn TP, Schlueter M, Soifer SJ, Gutierrez JA: Mechanotransduction in the lung-cyclic mechanical stretch induces VEGF and FGF-2 expression in pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2002;282:L897-L903
63. Hasaneen NA, Zucker S, Lin RZ, Vaday GG, Panettieri RA, Foda HD: Angiogenesis is induced by airway smooth muscle strain. Am J Physiol Lung Cell Mol Physiol 2007;293:L1059-L1068
64. Xu J, Liu MY, Liu J, Caniggia I, Post M: Mechanical strain induces constitutive and regulated secretion of glycosaminoglycans and proteoglycans in fetal lung cells. J Cell Sci 1996;109:1605-1613
65. Mourgeon E, Xu J, Tanswell AK, Liu MY, Post M: Mechanical strain-induced posttranscriptional regulation of fibronectin production in fetal lung cells. Am J Physiol Lung Cell Mol Physiol 1999;277:L142-L149
66. Swartz MA, Tschumperlin DJ, Kamm RD, Drazen JM: Mechanical stress is communicated between different cell types to elicit matrix remodeling. Proc Natl Acad Sci USA 2001;98:6180-6185
67. Hendricks P, Diaz F, Schmitt S, Sittampalam GS, Nirmalanandhan VS: Effects of respiratory mechanical forces on the pharmacological response of lung cancer cells to chemotherapeutic agents. Fundam Clin Pharmacol 2011 Jul 1 [Epub ahead of print]. doi:10.1111/j.1472-8206.2011.00964.x
68. Gutierrez JA, Suzara VV, Dobbs LG: Continuous mechanical contraction modulates expression of alveolar epithelial cell phenotype. Am J Respir Cell Mol Biol 2003;29:81-87
69. Wang YL, Maciejewski BS, Soto-Reyes D, Lee HS, Warburton D, Sanchez- Esteban J: Mechanical stretch promotes fetal type II epithelial cell differentiation via shedding of HB-EGF and TGF-alpha. J Physiol 2009;587: 1739-1753
70. Copland IB, Kavanagh BP, Engelberts D, McKerlie C, Belik J, Post M: Early changes in lung gene expression due to high tidal volume. Am J Respir Crit Care Med 2003;168:1051-1059
71. Vlahakis NE, Schroeder MA, Limper AH, Hubmayr RD: Stretch induces cytokine release by alveolar epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 1999;277:L167-L173
72. Yamamoto H, Teramoto H, Uetani K, Igawa K, Shimizu E: Cyclic stretch upregulates interleukin-8 and transforming growth factor-beta 1 production through a protein kinase C-dependent pathway in alveolar epithelial cells. Respirology 2002;7:103-109
73. Quinn D, Tager A, Joseph PM, Bonventre JV, Force T, Hales CA: Stretch-induced mitogen-activated protein kinase activation and interleukin-8 production in type II alveolar cells. Chest 1999;116(Suppl 1):89S-90S
74. Oudin S, Pugin M: Role of MAP kinase activation in interleukin-8 production by human BEAS-2B bronchial epithelial cells submitted to cyclic stretch. Am J Respir Cell Mol Biol 2002;27:107-114
75. Li LF, Ouyang B, Choukroun G, et al.: Stretch-induced IL-8 depends on c-Jun NH2-terminal and nuclear factor-kappa B-inducing kinases. Am J Physiol Lung Cell Mol Physiol 2003;285:L464-L475
76. Mourgeon E, Isowa N, Keshavjee S, Zhang XM, Slutsky AS, Liu MY: Mechanical stretch stimulates macrophage inflammatory protein-2 secretion from fetal rat lung cells. Am J Physiol Lung Cell Mol Physiol 2000;279:L699-L706
77. Savla U, Waters CM: Mechanical strain inhibits repair of airway epithelium in vitro. Am J Physiol Lung Cell Mol Physiol 1998;274:L883-L892
78. Desai LP, White SR, Waters CM: Cyclic mechanical stretch decreases cell migration by inhibiting phosphatidylinositol 3-kinase- and focal adhesion kinase-mediated JNK1 activation. J Biol Chem 2009;285:4511-4519
79. Pugin J, Dunn-Siegrist I, Dufour J, Tissieres P, Charles PE, Comte R: Cyclic stretch of human lung cells induces an acidification and promotes bacterial growth. Am J Respir Cell Mol Biol 2008;38:362-370
80. Waters CM, Ridge KM, Sunio G, Venetsanou K, Sznajder JI: Mechanical stretching of alveolar epithelial cells increases Na + -K + -ATPase activity. J Appl Physiol 1999;87:715-721
81. Jedrych E, Ziolkowska K, Chudy M, Brzozka Z: Microfluidic device for cell culture. Przeglad Elektrotechniczny 2010;86:33-35
82. Jemal A, Siegel R, Ward E, Hao YP, Xu JQ, Thun MJ: Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-249
83. Onn A, Isobe T, Itasaka S, et al.: Development of an orthotopic model to study the biology and therapy of primary human lung cancer in nude mice. Clin Cancer Res 2003;9:5532-5539
84. Wu WJ, Onn A, Isobe T, et al.: Targeted therapy of orthotopic human lung cancer by combined vascular endothelial growth factor and epidermal growth factor receptor signaling blockade. Mol Cancer Ther 2007;6:471-483
85. Onn A, Isobe T, Wu WJ, et al.: Epidermal growth factor receptor tyrosine kinase inhibitor does not improve paclitaxel effect in an orthotopic mouse model of lung cancer. Clin Cancer Res 2004;10:8613-8619
86. Erlichman C, Hidalgo M, Boni JP, et al.: Phase I study of EKB-569, an irreversible inhibitor of the epidermal growth factor receptor, in patients with advanced solid tumors. J Clin Oncol 2006;24:2252-2260
87. Chu EK, Foley JS, Cheng J, Patel AS, Drazen JM, Tschumperlin DJ: Bronchial epithelial compression regulates epidermal growth factor receptor family ligand expression in an autocrine manner. Am J Respir Cell Mol Biol 2005; 32:373-380
88. Papaiahgari S, Yerrapureddy A, Hassoun PM, Garcia JG, Birukov KG, Reddy SP: EGFR-activated signaling and actin remodeling regulate cyclic stretch-induced NRF2-ARE activation. Am J Respir Cell Mol Biol 2007;36:304-312
89. Lam AP, Dean DA: Cyclic stretch-induced nuclear localization of transcription factors results in increased nuclear targeting of plasmids in alveolar epithelial cells. J Gene Med 2008;10:668-678
90. Geiger RC, Taylor W, Glucksberg MR, Dean DA: Cyclic stretch-induced reorganization of the cytoskeleton and its role in enhanced gene transfer. Gene Ther 2006;13:725-731
91. Cohen TS, Cavanaugh KJ, Margulies SS: Frequency and peak stretch magnitude affect alveolar epithelial permeability. Eur Respir J 2008;32:854-861
92. Birukov KG, Jacobson JR, Flores AA, et al.: Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol Lung Cell Mol Physiol 2003;285:L785-L797
93. Birukova AA, Fu PF, Xing JJ, Yakubov B, Cokic I, Birukov KG: Mechanotransduction by GEF-H1 as a novel mechanism of ventilatorinduced vascular endothelial permeability. Am J Physiol Lung Cell Mol Physiol 2010;298:L837-L848
94. Cavanaugh KJ, Oswari J, Margulies SS: Role of stretch on tight junction structure in alveolar epithelial cells. Am J Respir Cell Mol Biol 2001;25:584-591
95. Cavanaugh KJ, Cohen TS, Margulies SS: Stretch increases alveolar epithelial permeability to uncharged micromolecules. Am J Physiol Cell Physiol 2006; 290:C1179-C1188
96. Rehfeldt F, Engler AJ, Eckhardt A, Ahmed F, Discher DE: Cell responses to the mechanochemical microenvironment-implications for regenerative medicine and drug delivery. Adv Drug Deliv Rev 2007;59:1329-1339
97. Brown XQ, Bartolak-Suki E, Williams C, Walker ML, Weaver VM, Wong JY: Effect of substrate stiffness and PDGF on the behavior of vascular smooth muscle cells: implications for atherosclerosis. J Cell Physiol 2010;225:115-122
98. Liu F, Mih JD, Shea BS, et al.: Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 2010;190:693-706
99. Lam WA, Cao L, Umesh V, Keung AJ, Sen S, Kumar S: Extracellular matrix rigidity modulates neuroblastoma cell differentiation and N-myc expression. Mol Cancer 2010;9:35
100. Krishnan R, Klumpers DD, Park CY, et al.: Substrate stiffening promotes endothelial monolayer disruption through enhanced physical forces. Am J Physiol Cell Physiol 2011;300:C146-C154
101. Tilghman RW, Cowan CR, Mih JD, et al.: Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS One 2010;5:e12905
102. Paszek MJ, Zahir N, Johnson KR, et al.: Tensional homeostasis and the malignant phenotype. Cancer Cell 2005;8:241-254
103. Kirstein MN, Wieman KM, Williams BW, et al.: Short versus continuous gemcitabine treatment of non-small cell lung cancer in an in vitro cell culture bioreactor system. Lung Cancer 2007;58:196-204
104. Kirstein MN, Brundage RC, Moore MM, et al.: Pharmacodynamic characterization of gemcitabine cytotoxicity in an in vitro cell culture bioreactor system. Cancer Chemother Pharmacol 2008;61:291-299
105. Moraes C, Wang GH, Sun Y, Simmons CA: A microfabricated platform for high-throughput unconfined compression of micropatterned biomaterial arrays. Biomaterials 2010;31:577-584