Postoperative-fluid retention is a severe complication frequently reported in patients undergoing major surgical procedures. The complex network of molecules involved in such a severe surgery-induced condition remains poorly understood. Inflammation has been proposed among the various causes of fluid retention. Since TNF-α is one of the main proinflammatory cytokine initially released after major surgery, it is reasonable to assume its involvement in fluid overload. Here, we showed that TNF-α selectively regulates key molecules involved in fluids balance, such as natriuretic peptides (NPs) and aquaporins, in human bronchial epithelial cells BEAS-2B. In particular, we found that TNF-α induced a decrease of arial natriuretic peptide, natriuretic peptide receptor-1, aquaporin-1 and aquaporin-5 and an increase of brain natriuretic peptide with a different involvement of nuclear factor-κB and mitogen-activated protein kinases signaling pathway activation. Moreover, the observed changes in NPs expression, demonstrate inflammation as an additional cause of brain natriuretic peptide elevation, adding an important piece of information in the novel area of study regarding NPs and inflammation. Finally, we suggest that inflammation is one of the mechanisms of Aquaporin-1 and aquaporin-5 expression regulation. Therefore, in this exploratory study, we speculate that TNF-α might be involved in postoperative-fluid retention related to major surgery. 1. Introduction Weight gain with edema formation is frequently reported in patients undergoing major surgical procedures, with an incidence as high as 40% [1]. Postoperative weight gain and fluid overload have been associated with poor survival [2] and complications [3, 4]. The causes of fluid retention are various, and not completely clear. One of them could be related to the systemic response induced by surgical stress and operative trauma, regulated by a complex network of endocrine, neuronal, and immunological mechanisms [5–7]. Such surgery-induced reaction leads to an early hyperinflammatory status that is essential for tissue repair and host defense [5]. Cytokines are thought to play a pivotal role in the pathogenesis of surgical trauma. They have local effects of mediating and maintaining the inflammatory response to tissue injury and also initiate some of the systemic changes which occur [8–10]. After major surgery, is one of the main proinflammatory cytokines initially released in the damaged tissue where it stimulates the production and release of more cytokines, responsible for inducing the systemic changes
References
[1]
E. Itobi, M. Stroud, and M. Elia, “Impact of oedema on recovery after major abdominal surgery and potential value of multifrequency bioimpedance measurements,” The British Journal of Surgery, vol. 93, no. 3, pp. 354–361, 2006.
[2]
J. A. Lowell, C. Schifferdecker, D. F. Driscoll, P. N. Benotti, and B. R. Bistrian, “Postoperative fluid overload: not a benign problem,” Critical Care Medicine, vol. 18, no. 7, pp. 728–733, 1990.
[3]
A. M. M？ller, T. Pedersen, P.-E. Svendsen, and A. Engquist, “Perioperative risk factors in elective pneumonectomy: the impact of excess fluid balance,” European Journal of Anaesthesiology, vol. 19, no. 1, pp. 57–62, 2002.
[4]
E. Bennett-Guerrero, D. E. Feierman, G. R. Barclay et al., “Preoperative and intraoperative predictors of postoperative morbidity, poor graft function, and early rejection in 190 patients undergoing liver transplantation,” Archives of Surgery, vol. 136, no. 10, pp. 1177–1183, 2001.
[5]
J. P. Desborough, “The stress response to trauma and surgery,” The British Journal of Anaesthesia, vol. 85, no. 1, pp. 109–117, 2000.
[6]
H. Tsujimoto, S. Ono, T. Majima et al., “Differential toll-like receptor expression after ex vivo lipopolysaccharide exposure in patients with sepsis and following surgical stress,” Clinical Immunology, vol. 119, no. 2, pp. 180–187, 2006.
[7]
C. Evans, C. Galustian, D. Kumar et al., “Impact of surgery on immunologic function: comparison between minimally invasive techniques and conventional laparotomy for surgical resection of colorectal tumors,” The American Journal of Surgery, vol. 197, no. 2, pp. 238–245, 2009.
[8]
F. Catena, L. Ansaloni, A. Avanzolini et al., “Systemic cytokine response after emergency and elective surgery for colorectal carcinoma,” International Journal of Colorectal Disease, vol. 24, no. 7, pp. 803–808, 2009.
[9]
R. Sarbinowski, S. Arvidsson, M. Tylman, T. ？resland, and A. Bengtsson, “Plasma concentration of procalcitonin and systemic inflammatory response syndrome after colorectal surgery,” Acta Anaesthesiologica Scandinavica, vol. 49, no. 2, pp. 191–196, 2005.
[10]
P. Sheeran and G. M. Hall, “Cytokines in anaesthesia,” The British Journal of Anaesthesia, vol. 78, no. 2, pp. 201–219, 1997.
[11]
L. Cagini, R. Capozzi, V. Tassi et al., “Fluid and electrolyte balance after major thoracic surgery by bioimpedance and endocrine evaluation,” European Journal of Cardio-Thoracic Surgery, vol. 40, no. 2, pp. e71–e76, 2011.
[12]
T. Omland and T. Hagve, “Natriuretic peptides: physiologic and analytic considerations,” Heart Failure Clinics, vol. 5, no. 4, pp. 471–487, 2009.
[13]
L. R. Potter, A. R. Yoder, D. R. Flora, L. K. Antos, and D. M. Dickey, “Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications,” Handbook of Experimental Pharmacology, vol. 191, pp. 341–366, 2009.
[14]
T. G. Flynn, M. L. de Bold, and A. J. de Bold, “The amino acid sequence of an atrial peptide with potent diuretic and natriuretic properties,” Biochemical and Biophysical Research Communications, vol. 117, no. 3, pp. 859–865, 1983.
[15]
A. J. de Bold, “Atrial natriuretic factor: a hormone produced by the heart,” Science, vol. 230, pp. 767–770, 1985.
[16]
K. Kangawa, Y. Tawaragi, S. Oikawa et al., “Identification of rat γ atrial natriuretic polypeptide and characterization of the cDNA encoding its precursor,” Nature, vol. 312, no. 5990, pp. 152–155, 1984.
[17]
T. Sudoh, K. Kangawa, N. Minamino, and H. Matsuo, “A new natriuretic peptide in porcine brain,” Nature, vol. 332, no. 6159, pp. 78–81, 1988.
[18]
M. Kuhn, “Endothelial actions of atrial and B-type natriuretic peptides,” The British Journal of Pharmacology, vol. 166, no. 2, pp. 522–531, 2012.
[19]
A. J. de Bold, “Cardiac natriuretic peptides gene expression and secretion in inflammation,” Journal of Investigative Medicine, vol. 57, pp. 29–32, 2009.
[20]
S. P. D'Souza, M. Davis, and G. F. Baxter, “Autocrine and paracrine actions of natriuretic peptides in the heart,” Pharmacology and Therapeutics, vol. 101, no. 2, pp. 113–129, 2004.
[21]
M. Brueckmann, G. Huhle, S. Lang et al., “Prognostic value of plasma N-terminal pro-brain natriuretic peptide in patients with severe sepsis,” Circulation, vol. 112, no. 4, pp. 527–534, 2005.
[22]
J. Charpentier, C. E. Luyt, Y. Fulla et al., “Brain natriuretic peptide: a marker of myocardial dysfunction and prognosis during severe sepsis,” Critical Care Medicine, vol. 32, no. 3, pp. 660–665, 2004.
[23]
R. Shor, Y. Rozenman, A. Bolshinsky et al., “BNP in septic patients without systolic myocardial dysfunction,” European Journal of Internal Medicine, vol. 17, no. 8, pp. 536–540, 2006.
[24]
T. Inoue, M. Kawai, T. Nakane et al., “Influence of low-grade inflammation on plasma B-type natriuretic peptide levels,” Internal Medicine, vol. 49, no. 24, pp. 2659–2668, 2010.
[25]
P. Agre, L. S. King, M. Yasui et al., “Aquaporin water channels—from atomic structure to clinical medicine,” Journal of Physiology, vol. 542, no. 1, pp. 3–16, 2002.
[26]
P. Agre and D. Kozono, “Aquaporin water channels: molecular mechanisms for human diseases,” FEBS Letters, vol. 555, no. 1, pp. 72–78, 2003.
[27]
J. M. Carbrey and P. Agre, “Discovery of the aquaporins and development of the field,” Handbook of Experimental Pharmacology, vol. 190, pp. 3–28, 2009.
[28]
O. Bloch and G. T. Manley, “The role of aquaporin-4 in cerebral water transport and edema,” Neurosurgical Focus, vol. 22, no. 5, article E3, 2007.
[29]
J. Li, M. Xu, Q. Fan et al., “Tanshinone IIA ameliorates seawater exposure-induced lung injury by inhibiting aquaporins (AQP) 1 and AQP5 expression in lung,” Respiratory Physiology and Neurobiology, vol. 176, no. 1-2, pp. 39–49, 2011.
[30]
J. E. Towne, K. S. Harrod, C. M. Krane, and A. G. Menon, “Decreased expression of aquaporin (AQP)1 and AQP5 in mouse lung after acute viral infection,” The American Journal of Respiratory Cell and Molecular Biology, vol. 22, no. 1, pp. 34–44, 2000.
[31]
J. E. Towne, C. M. Krane, C. J. Bachurski, and A. G. Menon, “Tumor necrosis factor-α inhibits aquaporin 5 expression in mouse lung epithelial cells,” The Journal of Biological Chemistry, vol. 276, no. 22, pp. 18657–18664, 2001.
[32]
K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001.
[33]
K. Verhelst, I. Carpentier, and R. Beyaert, “Regulation of TNF-induced NF-κB activation by different cytoplasmic ubiquitination events,” Cytokine and Growth Factor Reviews, vol. 22, no. 5-6, pp. 277–286, 2011.
[34]
L. Qian, Y. Shen, J. C. Chen et al., “3D-QSAR and docking studies of quinazoline derivatives with the inhibatory activity toward NF-κB,” QSAR and Combinatorial Science, vol. 27, no. 8, pp. 984–995, 2008.
[35]
P. D. N'Guessan, S. Hippenstiel, M. O. Etouem et al., “Streptococcus pneumoniae induced p38 MAPK- and NF-κB-dependent COX-2 expression in human lung epithelium,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 290, no. 6, pp. L1131–L1138, 2006.
[36]
B. Schmeck, K. Moog, J. Zahlten et al., “Streptococcus pneumoniae induced c-Jun-N-terminal kinase- and AP-I-dependent IL-8 release by lung epithelial BEAS-2B cells,” Respiratory Research, vol. 7, article 98, 2006.
[37]
M. G. Matera, L. Calzetta, D. Passeri et al., “Epithelium integrity is crucial for the relaxant activity of brain natriuretic peptide in human isolated bronchi,” The British Journal of Pharmacology, vol. 163, no. 8, pp. 1740–1754, 2011.
[38]
R. Quirion, M. Dalpe, A. de Lean, J. Gutkowska, M. Cantin, and J. Genest, “Atrial natriuretic factor (ANF) binding sites in brain and related structures,” Peptides, vol. 5, no. 6, pp. 1167–1172, 1984.
[39]
M. B. Pamnani, D. L. Clough, J. S. Chen, W. T. Link, and F. J. Haddy, “Effects of rat atrial extract on sodium transport and blood pressure in the rat,” Proceedings of the Society for Experimental Biology and Medicine, vol. 176, no. 2, pp. 123–131, 1984.
[40]
T. R. Traynor and S. M. O'Grady, “Brain natriuretic peptide stimulates K and Cl secretion across porcine distal colon epithelium,” The American Journal of Physiology—Cell Physiology, vol. 260, no. 4, pp. C750–C755, 1991.
[41]
R. Rollín, A. Mediero, M. Roldán-Pallarés, A. Fernández-Cruz, and R. Fernández-Durango, “Natriuretic peptide system in the human retina,” Molecular Vision, vol. 10, pp. 15–22, 2004.
[42]
M. Harada, H. Itoh, O. Nakagawa et al., “Significance of ventricular myocytes and nonmyocytes interaction during cardiocyte hypertrophy: evidence for endothelin-1 as a paracrine hypertrophic factor from cardiac nonmyocytes,” Circulation, vol. 96, no. 10, pp. 3737–3744, 1997.
[43]
K. Kuwahara, Y. Saito, M. Harada et al., “Involvement of cardiotrophin-1 in cardiac myocyte-nonmyocyte interactions during hypertrophy of rat cardiac myocytes in vitro,” Circulation, vol. 100, no. 10, pp. 1116–1124, 1999.
[44]
E. Harada, O. Nakagawa, M. Yoshimura et al., “Effect of interleukin-1β on cardiac hypertrophy and production of natriuretic peptides in rat cardiocyte culture,” Journal of Molecular and Cellular Cardiology, vol. 31, no. 11, pp. 1997–2006, 1999.
[45]
V. Chiurchiù, V. Izzi, F. D'Aquilio, F. Carotenuto, P. Di Nardo, and P. M. Baldini, “Brain natriuretic peptide (BNP) regulates the production of inflammatory mediators in human THP-1 macrophages,” Regulatory Peptides, vol. 148, no. 1–3, pp. 26–32, 2008.
[46]
N. S. Holden, C. F. Rider, M. J. Bell et al., “Enhancement of inflammatory mediator release by β2-adrenoceptor agonists in airway epithelial cells is reversed by glucocorticoid action,” The British Journal of Pharmacology, vol. 160, no. 2, pp. 410–420, 2010.
[47]
V. S. Fang, C. C. Juan, J. G. S. Won, and L. T. Ho, “Further study of aldosterone secretion-inhibitory factor and brain natriuretic peptide on cortisol production of Guinea pig zona fasciculata cells,” Chinese Journal of Physiology, vol. 43, no. 4, pp. 141–147, 2000.
[48]
G. Hellermann, X. Kong, J. Gunnarsdóttir et al., “Mechanism of bronchoprotective effects of a novel natriuretic hormone peptide,” Journal of Allergy and Clinical Immunology, vol. 113, no. 1, pp. 79–85, 2004.
[49]
K. K. Ma, T. Ogawa, and A. J. de Bold, “Selective upregulation of cardiac brain natriuretic peptide at the transcriptional and translational levels by pro-inflammatory cytokines and by conditioned medium derived from mixed lymphocyte reactions via p38 MAP kinase,” Journal of Molecular and Cellular Cardiology, vol. 36, no. 4, pp. 505–513, 2004.
[50]
T. Ogawa, J. P. Veinot, M. L. K. de Bold, T. Georgalis, and A. J. De Bold, “Angiotensin II receptor antagonism reverts the selective cardiac BNP upregulation and secretion observed in myocarditis,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 294, no. 6, pp. H2596–H2603, 2008.
[51]
B. J. Carver, E. J. Plosa, A. M. Stinnett, T. S. Blackwell, and L. S. Prince, “Interactions between NF-κB and SP3 connect inflammatory signaling with reduced FGF-10 expression,” The Journal of Biological Chemistry, vol. 288, no. 21, pp. 15318–15325, 2013.
[52]
C. Dong, G. Wang, B. Li et al., “Anti-asthmatic agents alleviate pulmonary edema by upregulating AQP1 and AQP5 expression in the lungs of mice with OVA-induced asthma,” Respiratory Physiology and Neurobiology, vol. 181, no. 1, pp. 21–28, 2012.
