Extraordinarily high aldosterone, ng/dl, in a patient with primary aldosteronism: an insight into the underlying mechanism
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1 2016, 63 (2), Original Extraordinarily high aldosterone, ng/dl, in a patient with primary aldosteronism: an insight into the underlying mechanism Yosuke Okubo 1), Yuka Sato 2), Yasuto Nakasone 2), Katsuko Shirotori 3), Kazuhiro Oguchi 4), Tsuyoshi Matsushita 5), Tetsuo Nishikawa 6), Yuto Yamazaki 7), Hironobu Sasano 7), Mitsuhisa Komatsu 1), Keishi Yamauchi 2) and Toru Aizawa 2) 1) Division of Diabetes, Endocrinology and Metabolism, Department of Internal Medicine, Shinshu University School of Medicine, Matsumoto, Japan 2) Diabetes Center, Aizawa Hospital, Matsumoto, Japan 3) Department of Nephrology, Aizawa Hospital, Matsumoto, Japan 4) Positron Imaging Center, Aizawa Hospital, Matsumoto, Japan 5) Department of Radiology, Shinshu University School of Medicine, Matsumoto, Japan 6) Endocrinology and Diabetes Center, Yokohama Rosai Hospital, Yokohama, Japan 7) Department of Pathology, Tohoku University Graduate School of Medicine, Sendai, Japan Abstract. A 43-yr-old hypertensive male was admitted due to hypokalemia (1.8 meq/l) and renal dysfunction (egfr, 20.0 ml/min/1.73 m 2 ). His plasma aldosterone was ng/dl, plasma renin activity 5.7 ng/ml/hr, and aldosterone/ renin activity ratio 158. Angiotensin II (AII) was 0.7 pg/ml, ACTH <1.0 pg/ml, and cortisol 21.6 μg/dl. Liquid chromatography-tandem mass spectrometry analysis showed that aldosterone (104 times the control) as well as its precursors were significantly elevated in the patient s plasma. A left adrenal (4-cm-diameter) tumor with 131 I-Adosterol uptake was found and removed. Four days later, plasma aldosterone and renin activity had dropped to 7.73 ng/dl and 1.6 ng/ml/hr, respectively. However, they rose to 24.0 ng/dl and 10.9 ng/ml/hr, respectively, by Day 102. Nevertheless, magnetic resonance angiography found no evidence of a renovascular lesion. The tumor was a benign adrenocortical adenoma composed predominantly of clear cells positive for 17α-hydroxylase, [hydroxy-delta-5-steroid dehydrogenase, 3 beta- and steroid delta-isomerases], and aldosterone synthase. A quantitative real-time polymerase chain reaction analysis of the tumor cells revealed that expression of the gene encoding aldosterone synthase was 85 times the control level. In addition, the tumor cells harbored G151R mutation of the inward rectifying potassium channel subfamily j, member 5 gene. The striking overexpression of aldosterone synthase by the tumor cells was considered the primary mechanism for the extravagant overproduction of aldosterone in this case. This overexpression may have resulted from integration of signals from AII and forced membrane depolarization due to the potassium channel mutation. Key words: Aldosteronoma, Hyperreninemia, KCNJ5 mutation IN PRIMARY ALDOSTERONISM (PA), plasma renin activity (PRA) is suppressed, plasma aldosterone concentration (PAC) elevated, and PAC/ PRA ratio high [1, 2]. However, we encountered an unusual patient with astonishingly high PAC with elevated PRA. We performed an extensive clinical, pathological and molecular analysis in this case in search of underlying mechanism for the striking overproduc- Submitted Jul. 10, 2015; Accepted Oct. 15, 2015 as EJ Released online in J-STAGE as advance publication Nov. 7, 2015 Correspondence to: Toru Aizawa, Diabetes Center, Aizawa Hospital, Honjo, Matsumoto , Japan. taizawax@ai-hosp.or.jp Y.O. and Y.S. are co-first authors. The Japan Endocrine Society tion of aldosterone by the tumor. Case Report A 43-yr-old man was admitted due to hypokalemia. He has been hypertensive for 10 yrs and renal dysfunction has been documented for the previous 2 yrs. His BMI was 20.5 kg/m 2, BP 120/80 mmhg with 5 mg amlodipine, and pulse rate 110/min, irregular. ECG revealed frequent premature ventricular contractions. There was no edema or muscle weakness, but the patient had profound hypokalemia (1.8 meq/l), metabolic alkalosis and renal dysfunction (estimated glomerular filtration rate, egfr 20.0 ml/min/1.73 m 2 )
2 128 Okubo et al. (Table 1). Urinary potassium excretion was high (25.1 meq/g.creatinine) relative to the hypokalemia. PAC was surprisingly high (901.0 ng/dl), and PRA (5.7 ng/ ml/hr) and angiotensin II (AII) (0.70 pg/ml) unexpectedly elevated. The PAC to PRA ratio was 158 [ng/dl]/[ng/ml/hr]. ACTH was suppressed and cortisol slightly elevated both in the morning and at night. Plasma catecholamines were within the reference range except for a minimal elevation of dopamine, which was considered non-pathognomonic. Random sample plasma glucose was 146 mg/dl and HbA1c 6.2%. An abdominal CT-scan revealed a low density left adrenal tumor (ca. 4 cm in diameter) (Fig. 1) with a selective uptake of 131 I-Adosterol (Supplemental Fig. 1). The right adrenal gland appeared normal. The hypokalemia was corrected by the administration of spironolactone and potassium chloride, and the arrhythmia disappeared. The tumor, which was removed by a laparoscopic operation, was found to be composed of clear cells with a low Ki-67 index (2%), and judged to be benign [3]. PAC and PRA had dropped to 7.73 ng/dl and 1.6 ng/ml/hr, respectively, by postoperative Day 4, but rose to ng/dl and 9.6 ng/ml/hr, respectively, by Day 42. They further rose to and 24.0 ng/dl and 10.9 ng/ml/hr, respectively, by Day 102 and lowered to 17.6 ng/dl and 4.9 ng/ml/hr by Day 196 (Table 1). One hundred ninety-six days after the surgery, the morning plasma ACTH and cortisol were 34.6 pg/ml and 8.9 μg/dl, respectively. Methods Measurement of preoperative plasma steroids by liquid chromatography-tandem mass spectrometry (LC-MS/MS) was performed at ASKA Pharmaceutical (Tokyo). Immunohistochemical analysis of the steroidogenic enzymes of the tumor specimen was performed as described previously [4]. Expression of the genes encoding steroidogenic enzymes, AII receptor and ACTH receptor was determined by quantitative real-time polymerase chain reaction (RT-qPCR) [5]. Sequencing of the inward rectifying potassium channel subfamily j, member 5 gene (KCNJ5) was carried out as reported previously [6]. Postoperatively, configuration of the renal arteries was examined by magnetic resonance angiography. Results Plasma steroids determined by LC-MS/MS Aldosterone was drastically elevated in the patient s plasma (104 times the control), and its precursors such as deoxycorticosterone (24 times), corticosterone (7.7 times) and 18-hydroxy-corticosterone (47 times), were also elevated, albeit less significantly (Supplemental Fig. 2). The plasma concentration of progesterone (a common precursor of aldosterone and cortisol) was also significantly elevated (13 times) in the patient. However, cortisol per se was only 1.8 times the control. Immunohistochemistry The tumor cells were immunohistochemically positive for 17α-hydroxylase (CYP17) (Fig. 2A), [hydroxydelta-5-steroid dehydrogenase, 3 beta- and steroid delta-isomerase 1 and 2] (HSD3B1 and B2) (Fig. 2B for HSD3B2) and [cytochrome P450, family 11, subfam- Fig. 1 A. Abdominal CT scan taken before the operation. The arrow indicates a low density (7.7 Hounsfield Unit) left adrenal tumor. B. Magnetic resonance angiography of the renal arteries.
3 Extraordinarily high aldosterone in PA 129 Table 1 Clinical data Variable (Reference range) Before operation With correction of On admission hypokalemia After operation Day 4 Day 42 Day 105 Day 196 Blood pressure, mmhg 120/80 116/72-133/90 127/72 149/ /96 152/96 Body weight, kg Hormone PAC, ng/dl ( ) PRA, ng/ml/hr, ( ) PAC/PRA ratio (<20) AII, pg/ml (<0.35) ACTH, pg/ml ( ) 6:00/23:00 1.7/ < * 34.3** Cortisol, μg/dl ( ) 6:00/23: / * 8.9** Catecholamines, pg/ml Epinephrine (<0.1) <0.01 Norepinephrine ( ) 0.27 Dopamine (<0.02) 0.08 Chemistry K, meq/l ( ) Na, meq/l ( ) SCr, mg/dl ( ) egfr, ml/min/1.73 m Urine chemistry K, meq/l Na, meq/l Cr, mg/dl Medication 5 mg amlodipine mg spironolactone, 0.31 mg bisoprolol fumarate, 7.2 g pottasium chloride 0.31 mg bisoprolol fumarate, 30 mg hydrocortisone 0.31 mg bisoprolol fumarate 2.5 mg amlodipine PAC, plasma aldosterone concentration; PRA, plasma renin activity; AII, angiotensin II; Scr, serum creatinine; egfr, estimated glomerular filtration rate; Cr, creatinine; * The morning sample, receiving 10 mg hydrocortisone po three times a day to prevent adrenal insufficiency. ** Morning sample, not receiving hydrocortisone. The reference range is shown in the parentheses. Aldosterone, cortisol PRA, AII and catecholamines were determined at Special Reference Laboratory (Tokyo). Fig. 2 Immunohistochemistry of the tumor cells. A. 17α-hydroxylase (CYP17) B. hydroxy-delta-5-steroid dehydrogenase, 3 beta- and steroid delta-isomerase 1 (HSD3B1) C. cytochrome P450, family 11, subfamily B, polypeptide 2 (CYP11B2, aldosterone synthase)
4 130 Okubo et al. Table 2 RT-qPCR of the tumor tissue Gene Sample StAR P450 SCC HSD3B2 HSD3B1 CYP17A1 CYP11B1 CYP11B2 AGTR1 MC2R Tumor of the patient Nonfunctioning tumor # Control Nonfunctioning tumor # RT-qPCR, quantitative real-time polymerase chain reaction; StAR, steroidogenic acute regulatory (StAR) protein; P450 SCC, cytochrome P450 cholesterol side-chain cleavage enzyme; HSD3B2, 3 beta-hydroxy-delta 5-steroid dehydrogenase/3-keto-delta 5-steroid isomerase 2; HSD3B1, 3 beta-hydroxy-delta 5-steroid dehydrogenase/3-keto-delta 5-steroid isomerase 1; CYP17A1, cytochrome P450, family 17, subfamily A, polypeptide 1; CYP11B1, cytochrome P450, family 11, subfamily B, polypeptide 1; CYP11B2, cytochrome P450, family 11, subfamily B, polypeptide 2; AGTR1, angiotensin II type 1 receptor; MC2R, melanocortin receptor 2 (ACTH receptor). Quantitative normalization of mrna was performed using the level of expression of glyceraldehyde 3-phosphate dehydrogenase gene as an internal control. The numbers for non-functioning tumors were assigned arbitrarily. dialysis [9, 10], in whom mechanism of extraordinarily high PAC remained unclear. Seminal findings in our patient were as follows. Most importantly, there was an overexpression of HSD3B1 (7.9 times the control) and CYP11B2 (85 times the control) in the tumor cells, the genes encoding the two rate-limiting enzymes for aldosterone synthesis [4]. Especially the overexpression of the latter was striking. Although overexpression of CYP11B2 per se is not uncommon in aldosteronoma [5], the degree of overexpression was exceptional in this case. Although there was a striking overexpression of CYP11B2, the tumor cell exhibited relatively low expression of CYP17, CYP11B1 and HSD3B2 compared to ordinary aldosteronomas or cortisol secreting aldosteronoma [5]. The overexpression of CYP11B2 may be attributable to the continuous stimulation of the tumor cells by elevated AII caused by augmented PRA [11]. Additionally, forced depolarization of the tumor cells due to G151R mutation of KCNJ5 must have contributed to the overexpression of CYP11B2 [12, 13]. Both hyperreninemic state with kidney damage [8, 14] and G151R mutation of KCNJ5 [6, 12, 13, 15, 16] in isolation have been reported in patients with PA, but thus far no study has ever reported occurrence of the two in the same patient. The intrarenal artery was not clearly visualized due to an absence of contrast enhancement. However, sustained elevation of renin even after removal of the tumor strongly indicated intrarenal ischemia as a cause of hyperreninemia. Stimulation of growth of aldosteronoma by KCNJ5 mutation is a matter of debate. It was reported to be the case in one study [15] but not in the other [16]. Although the correlation of size of the tumor and PAC was weak and insignificant [2], relatively large tumor size in this patient might have been related to the strikily B, polypeptide 2] (CYP11B2, aldosterone synthase) (Fig. 2C). Renin immunoreactivity was negative. RT-qPCR and sequencing of KCNJ5 CYP11B2 was markedly overexpressed (ca. 85 times) by the tumor cells compared to the non-functioning adrenal adenoma cells (Table 2). HSD3B1 was also overexpressed (7.9 times the control). A mutation of KCNJ5, glycine-to-arginine substitution at codon 151 (p.g151r), was present in the tumor cells (Supplemental Fig. 3). There was no overexpression of genes encoding receptors for AII and ACTH (Table 2). Configuration of the renal artery Apparent renovascular stenosis was not identified by magnetic resonance angiography (Fig. 1B). Because the intrarenal artery was not clearly visualized due to an absence of contrast enhancement, it was not possible to rule out intrarenal ischemia. Discussion The PAC cutoff for diagnosis of PA is 15 ng/dl in patients with a PAC/PRA [ng/dl]/[ng/ml/hr] ratio >20 [2], and the highest PAC documented was 180 ng/dl in a series of 101 patients with PA [2]. In other series of patients with PA, the highest PAC was ng/ dl [5-7]. Even in patients with PA with renal dysfunction in whom unsuppressed PRA takes place occasionally, the highest PAC documented was 68.4 ng/dl [8]. Surprisingly, PAC was ng/dl in this patient. This value in the peripheral circulation of the patient was even comparable to the values in the adrenal vein of typical patients with PA [2]. As far as we are aware, PAC higher than the value observed in this patient was reported only in two patients with PA on chronic hemo-
5 Extraordinarily high aldosterone in PA 131 ingly high PAC. The glucocorticoid excess in this case may also have contributed to excessively high PAC through increase in renin substrate [17]. Of note, aldosterone reportedly enhanced renin gene expression in juxtaglomerular cells at supraphysiological concentration (EC 50 between and 3,610.0 ng/ dl) [18]. It should be noted that our patient s PAC of ng/dl was well within the effective range for the paradoxical effect of aldosterone. If such a mechanism was indeed at work in this case, a positive feedback loop would have been formed between the reninangiotensin system and aldosterone, which might have resulted in a self-perpetuating, vicious circle. The profile of steroid hormones and their precursors in the patient s serum reflected the combined overexpression of HSD3B1 and CYP11B2 and the underexpression by the tumor cells of the genes encoding enzymes for cortisol biosynthesis. Although the genes encoding the enzymes for cortisol synthesis were not overexpressed, cortisol must have overproduced in this case due to large tumor size, i.e., increased mass of cortisol producing cells. Six months after the operation, the morning ACTH and cortisol were within the normal range, which confirmed the above hypothesis. Aldosteronomas co-secreting cortisol are not uncommon [5]. In this patient, ectopic renin production by the adrenal tumor [19] was excluded. In conclusion, our finding adds an important information concerning the regulation of aldosterone pro- duction in vivo. We reported for the first time a patient with an aldosteronoma who exhibited PAC as high as ng/dl and elevated PRA. Extraordinarily high PAC in this patient was considered due to the striking overexpression of CYP11B2 by the tumor cells, which was most likely caused by synergistic stimulation by elevated AII and forced membrane depolarization arising from the KCNJ5 mutation. The K channel mutation might have stimulated tumor growth, and further exaggerated aldosterone overproduction. Moreover, paradoxical stimulation of renin by aldosterone might have been involved. It is such integration of signals at the level of aldosterone synthase [11] that may explain how the striking overproduction of aldosterone showed up. Acknowledgments We thank Drs J. Mori and H. Miura for donating their blood samples for steroid measurement. This work was supported by a Grant for Comprehensive Research on Life-Style Related Diseases including Cardiovascular Diseases and Diabetes Mellitus (H25-016) and by a Grant for Research on Intractable Diseases from the Ministry of Health, Labour and Welfare of Japan. Disclosure None of the authors have any potential conflicts of interest associated with this research. Supplemantal Fig I-Adosterol scintigraphy. SPECT/CT-scintigraphy (A) and planer scintigraphy (B) are shown. R, right side; Ant, anterior view; Post, posterior view.
6 132 Okubo et al. Supplemental Fig. 2 Plasma concentration of steroid hormones and their precursors determined by LC-MS/MS. The values were expressed as [concentration in the patient s plasma]/[the mean concentration of the control subjects (n=2)]. The controls were healthy male doctors at the age of 43 and 45. Substances which were more than 5 times higher in the patient are designated by red. The determination was performed at ASKA pharmaceutical, Tokyo, Japan. The unit of measure was pg/ml except for aldosterone which was expressed in ng/dl, and testosterone, cortisol, corticosterone, and 18-OH-corticosterone which were expressed in ng/ml. DOC, deoxycorticosterone; DHEA, dehydroepiandrosterone; CYP 21, steroid 21-hydroxylase; CYP 19, aromatase; HSD17B, hydroxysteroid (17β) dehydrogenases. For other abbreviations, see Table 2. This figure was adapted and modified from Ref. 4. Supplemental Fig. 3 G151R mutation of the KCNJ5 gene
7 Extraordinarily high aldosterone in PA 133 References 1. Hiramatsu K, Yamada T, Yukimura Y, Komiya I, Ichikawa K, et al. (1981) A screening test to identify aldosterone-producing adenoma by measuring plasma renin activity. Results in hypertensive patients. Arch Intern Med 141: Mattsson C, Young WF Jr (2006) Primary aldosteronism: diagnostic and treatment strategies. Nat Clin Pract Nephrol 2: Weiss LM, Bertagna X, Chrousos GP, Kawashima A, Kleihues P, et al. (2004) Tumours of the adrenal gland, In: DeLellis R, Lloyd R (eds) Pathology and Genetics of Tumors of Endocrine Organs (3 rd ed). IARC, Lyon: Nakamura Y, Felizola SJ, Satoh F, Konosu-Fukaya S, Sasano H (2014) Dissecting the molecular pathways of primary aldosteronism. Pathol Int 64: Sakuma I, Suematsu S, Matsuzawa Y, Saito J, Omura M, et al. (2013) Characterization of steroidogenic enzyme expression in aldosterone-producing adenoma: a comparison with various human adrenal tumors. Endocr J 60: Kitamoto T, Suematsu S, Matsuzawa Y, Saito J, Omura M, et al. (2015) Comparison of cardiovascular complications in patients with and without KCNJ5 gene mutations harboring aldosterone-producing adenomas. J Atheroscler Thromb 22: Komiya I, Yamada T, Takasu N, Asawa T, Akamine H, et al. (1997) An abnormal sodium metabolism in Japanese patients with essential hypertension, judged by serum sodium distribution, renal function and the renin-aldosterone system. J Hypertens 15: Catena C, Colussi G, Nadalini E, Chiuch A, Baroselli S, et al. (2007) Relationships of plasma renin levels with renal function in patients with primary aldosteronism. Clin J Am Soc Nephrol 2: Koshiyama H, Fujisawa T, Kuwamura N, Nakamura Y, Kanamori H, et al. (2003) A case of normoreninemic aldosterone-producing adenoma associated with chronic renal failure: case report and literature review. Endocrine 21: Ikoma A, Saito T, Murata M, Toyoshima H, Nakamura Y, et al. (2010) Bilateral aldosteronoma associated with secondary aldosteronism in a chronic hemodialysis subject. Intern Med 49: Spät A, Hunyady L (2004) Control of aldosterone secretion: a model for convergence in cellular signaling pathways. Physiol Rev 84: Velarde-Miranda C, Gomez-Sanchez EP, Gomez- Sanchez CE (2013) Regulation of aldosterone biosynthesis by the Kir3.4 (KCNJ5) potassium channel. Clin Exp Pharmacol Physiol 40: Monticone S, Hattangady NG, Nishimoto K, Mantero F, Rubin B, et al. (2012) Effect of KCNJ5 mutations on gene expression in aldosterone-producing adenomas and adrenocortical cells. J Clin Endocrinol Metab 97: E Oelkers W, Diederich S, Bähr V (2000) Primary hyperaldosteronism without suppressed renin due to secondary hypertensive kidney damage. J Clin Endocrinol Metab 85: , Azizan EA, Lam BY, Newhouse SJ, Zhou J, Kuc RE, et al. (2012) Microarray, qpcr, and KCNJ5 Sequencing of aldosterone-producing adenomas reveal differences in genotype and phenotype between zona glom erulosaand zona fasciculata-like tumors. J Clin Endocrinol Metab 97: E Taguchi R, Yamada M, Nakajima Y, Satoh T, Hashimoto K, et al. (2012) Expression and mutations of KCNJ5 mrna in Japanese patients with aldosterone-producing adenomas. J Clin Endocrinol Metab 97: Saruta T (1996) Mechanism of glucocorticoid-induced hypertension. Hypertens Res 19: Klar J, Vitzthum H, Kurtz (2004) A Aldosterone enhances renin gene expression in juxtaglomerular cells. Am J Physiol Renal Physiol 286: F Kawai M, Sahashi K, Yamase H, Kishida Y, Sumida K, et al. (1998) Renin-producing adrenal tumor: report of a case. Surg Today 28:
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