Batabyal Dipanwita, Lewis-Ballester Ariel, Yeh Syun-Ru, Poulos Thomas L
Departments of Molecular Biology and Biochemistry, Chemistry, and Pharmaceutical Sciences, University of California , Irvine, California 92697, United States.
Department of Physiology and Biophysics, Albert Einstein College of Medicine , 1300 Morris Park Avenue, Bronx, New York 10461, United States.
Biochemistry. 2016 Nov 29;55(47):6517-6523. doi: 10.1021/acs.biochem.6b00913. Epub 2016 Nov 15.
The camphor monooxygenase, cytochrome P450cam, exhibits a strict requirement for its own redox partner, putidaredoxin (Pdx), a two-iron-sulfur ferredoxin. The closest homologue to P450cam, CYP101D1, is structurally very similar, uses a similar redox partner, and exhibits nearly identical enzymatic properties in the monooxygenation of camphor to give the same single 5-exo-hydroxy camphor product. However, CYP101D1 does not strictly require its own ferredoxin (Arx) for activity because Pdx can support CYP101D1 catalysis but Arx cannot support P450cam catalysis. We have further examined the differences between these two P450s by determining the effect of spin equilibrium, redox properties, and stability of oxygen complexes. We find that Arx shifts the spin state equilibrium toward high-spin, which is the opposite of the effect of Pdx on P450cam. In both P450s, redox partner binding destabilizes the oxy-P450 complex but this effect is much weaker with CYP101D1. In addition, resonance Raman data show that structural perturbations observed in P450cam upon addition of Pdx are absent in CYP101D1. These data indicate that Arx does not play the same effector role in catalysis as Pdx does with P450cam. The most relevant structural difference between these two P450s centers on a catalytically important Asp residue required for proton-coupled electron transfer. We postulate that with P450cam larger Pdx-assisted motions are required to free this Asp for catalysis while the smaller number of restrictions in CYP101D1 precludes the need for redox partner-assisted structural changes.
樟脑单加氧酶,即细胞色素P450cam,对其自身的氧化还原伴侣——恶臭假单胞菌铁氧还蛋白(Pdx,一种双铁硫铁氧还蛋白)有严格的需求。与P450cam最接近的同源物CYP101D1在结构上非常相似,使用相似的氧化还原伴侣,并且在樟脑单加氧反应中表现出几乎相同的酶学性质,生成相同的单一5-外向羟基樟脑产物。然而,CYP101D1的活性并不严格依赖其自身的铁氧还蛋白(Arx),因为Pdx可以支持CYP101D1的催化作用,而Arx不能支持P450cam的催化作用。我们通过测定自旋平衡、氧化还原性质和氧复合物稳定性的影响,进一步研究了这两种细胞色素P450之间的差异。我们发现Arx将自旋态平衡向高自旋方向移动,这与Pdx对P450cam的影响相反。在这两种细胞色素P450中,氧化还原伴侣的结合都会使氧-P450复合物不稳定,但这种影响在CYP101D1中要弱得多。此外,共振拉曼数据表明,添加Pdx后在P450cam中观察到的结构扰动在CYP101D1中不存在。这些数据表明,Arx在催化中所起的效应器作用与Pdx对P450cam所起的作用不同。这两种细胞色素P450之间最相关的结构差异集中在质子耦合电子转移所需的一个催化重要的天冬氨酸残基上。我们推测,对于P450cam,需要更大的Pdx辅助运动来释放这个天冬氨酸以进行催化,而CYP101D1中较少的限制使得不需要氧化还原伴侣辅助的结构变化。